The animal that moves makes its change of position by pressing against that which is beneath it…runners run faster if they swing their arms; for in the extension of the arms there is a kind of leaning upon the hands and wrists.
Aristotle (384-322 BC), On the Gait of Animals
It is likely that when you walked to your office this morning, you did not pay very much attention to what your arms and legs did to get you there. Smooth coordinated movement between the arms and legs are motor outputs that most people take completely for granted when they swim, walk, or run. We typically move our arms and legs in very regular and coordinated ways during locomotion. The interesting thing, however, is that we do not tend to attribute much importance to what our arms are actually doing while we walk. Subsequently, there is still uncertainty to whether arms are necessary for human locomotion. This is in marked contrast to what you might notice when walking your dog or watching your cat walk around the house. In those cases, it is very obvious and clear that both the forelimbs and the hindlimbs of those quadrupedal animals are intimately involved in producing locomotion. The point of this article is to argue that, despite these marked differences in the use of the forelimbs during bipedal and quadrupedal gait, quadrupedal neuronal linkages for forelimb and hind limb coordination during walking are conserved in humans. Many of these concepts have important implications for rehabilitation of movement after neurotrauma. This article is focused upon combining these elements and suggesting translational implications for rehabilitation based on these findings. That is, how can we usefully exploit our quadrupedal nature when needed for locomotor rehabilitation?
This article is concerned mostly with the locomotor activity of the cat, Old World Monkeys (e.g., vervet, macaque), chimpanzee, and human. A foundational working hypothesis is that innate neuronal networks providing the functional units of motor output for locomotion (spinal central pattern generators (CPG) (see review in (24))) are conserved across species. Related to this is the hypothesis that common core principles of motor control during locomotion are found in all four-limbed mammals. This is regardless of whether the mammal consistently walks on all four limbs (e.g., cats), locomotes with four limbs but uses the hindlimbs more for walking and the forelimbs more for swinging from branches and climbing (e.g., apes and chimpanzees), or walks on two limbs but also produces rhythmic motor patterns with all four limbs when walking and certainly when swimming and running (e.g., humans).
EVIDENCE FOR LINKAGES BETWEEN THE UPPER AND LOWER LIMBS
In the bipedal human, elements of quadrupedal coordination between arm and leg activity are likely conserved during locomotion (6,33). However, in human studies, it is impossible to obtain direct evidence for interlimb locomotor linkages. Instead, indirect evidence from reflex studies can be used as a tool to probe such neural activity. This allows for an approximation of the input-output properties of neural control during movement by applying a given sensory input and recording the pattern of modulation of motor output. This approach has been used to great effect in the quadrupedal locomotor system and also in the human (33). During walking, interlimb reflexes in both the arms and legs after stimulation of cutaneous nerves in the hand and foot are phase modulated during the walking cycle (33), implicating coupling between segmental CPG regulating arm and leg motion. Arm and leg coordination during walking, creeping, and swimming has also been ascribed to activity of coupled CPG (6).
The interaction between neuronal oscillators presumed to contribute to movement of the arms and legs can be estimated by examining coupling effects during human rhythmic movement. A coupling effect is operationally defined as a measurable effect of limb movement on background or reflex muscle activity in another limb (e.g., the effect of arm swing on activity in the legs). For example, rhythmic arm cycling is shown to significantly suppress soleus H-reflex amplitude by approximately 20% compared with when the legs are stationary (10). This is shown in Figure 1 where the active arm CPG are shown to modulate reflex amplitude in the legs. Recently, we examined the effects of rhythmic arm activity on background and cutaneous reflex electromyographic (EMG) modulation patterns during a task in which both the arms and legs were rhythmically active (i.e., arm and leg cycling (A&L)). Using this cycling paradigm as a surrogate for "reduced" walking (32) allows for the separation of arm and leg movement to determine the contributions of the arms and legs. Results show that reflex modulation during combined rhythmic A&L cycling is dominated by the legs. However, notably, there is still sensitivity to contributions from the arms (1). This is complimentary to observations in the neonatal rat preparation where an interplay between the cervical and lumbar pattern generators coordinate rhythmic movement of forelimbs and hindlimbs, with lumbar CPG playing a dominant role (16). This is taken as evidence for conservation of CPG mechanisms across mammalian tetrapods and is a predicted outcome for the interactions between CPG regulating arm and leg movement during human walking (8,31,33). Interestingly, the dominance of lumbar over cervical activity has also been intimated in a clever experiment conducted in humans. Sakamoto and colleagues (26) had participants perform arm cycling simultaneous with leg cycling and then asked them to make voluntary changes in cadence. Whereas leg cycling cadence was not affected by voluntary changes in arm cadence, arm cycling was significantly altered when leg cycling cadence was altered. These results suggest an ascending lumbocervical influence of leg activity on arm activity during rhythmic movement that is reminiscent of the results of Juvin et al. (16) previously described.
Evidence of functional propriospinal interlimb connections between the hindlimbs and forelimbs has been clearly demonstrated in the cat and in the neonatal rat (8). These experiments in the cat and rat confirm an interplay between the cervical and lumbar pattern generators in coordinating rhythmic movement of forelimbs and hindlimbs, with the direction of influence being both caudorostral and rostrocaudal. Similar coordinated coupling of rhythmic movements of the hindlimbs and forelimbs seen in both intact cats stepping overground and on a treadmill and during swimming and in decerebrate cats stepping on a treadmill, immersed in water ("swimming") and suspended in the air. These results suggest interlimb coupling mediated by long propriospinal pathways (Miller et al., 1975 cited in (33)). Comparable observations of coordinated coupling of the arms and legs during locomotor activities like walking, creeping, and swimming are also seen in humans (6). The frequency relationship was maintained between the limbs during all of these activities, which suggests that the neuronal circuits controlling arm and leg movements were coupled in a fashion consistent with two coupled oscillators.
Findings from reflex studies also confirm interlimb connections and are suggestive of coordinated activity of CPGs. During fictive locomotion in high spinal paralyzed cats, reflex activity in hind limb motoneurons evoked with forelimb nerve stimulation was distinctly dependent of the phase of the step cycle (27). Such interlimb reflex modulation patterns during rhythmic movement are similar to segmental reflex patterns observed in humans that have also been ascribed in part to CPG activity (6,25,33). During human locomotion, mechanical or electrical perturbations to the lower limb evoked responses in arm muscles (6,33). Similarly, stimulation to the superficial radial nerve in the arm evoked responses in leg muscles during locomotion (13). Rhythmic arm cycling movement affects EMG activation (9) and reflex activity (1,10) in leg muscles. Recent observations support the role for interlimb reflexes in corrective responses during locomotion (14). Interlimb reflexes evoked in arm muscles were generally facilitated during an unstable walking task (14). Despite the fact that the arms do not directly generate propulsion during human walking, evidence suggests that neuronal connections between the cervical and lumbar pattern generators are retained in bipedal humans. Interestingly, Preuschoft (22) has observed that primate forelimbs play crucial roles in making first contact with objects in the locomotor environment. Thus, like those of humans, primate forelimbs are not always directly involved in generating ground reaction forces, but they have other relevant roles in locomotion (i.e., ensuring stability during walking).This is particularly relevant in the arboreal environment.
CHARACTERISTICS OF THE COUPLING BETWEEN THE FORELIMBS AND HINDLIMBS
Interlimb neuronal linkages in humans are exquisitely sensitive to the task that is performed, and connectivity is enhanced when it is most relevant. For example, holding an earth-referenced handrail can alter cutaneous reflex amplitudes in muscles across the entire body (19). This effect of the rail depends on the walking task being performed. This suggests that transmission in segmental and interlimb reflex pathways is influenced by the stability demands (i.e., context) of each task while also being subject to specific gating according to the locomotor task. The plausible explanation for the shift in weighting is that neural pathways to these muscles are gated to incorporate the external environment (in this case, the hand rail) into an automatic recovery strategy. That is, these enhanced reflexes may have a role in gait correction, making use of the rail to restore stability.
Rhesus monkeys show interlimb coordination between hindlimbs and forelimbs, unlike other quadrupedal mammals, and instead share many features of human gait. Unlike in the cat where the strength of the coupling between the two forelimbs is similar to that seen in the hindlimbs (see work of Yamaguchi reviewed in (33)), the rhesus demonstrates more highly coordinated locomotor coupling in the lumbar segment than in cervical segments (4), a characteristic that may be similar in humans (1,34,35). In addition nonhuman primates use diagonal coordination between forelimbs and hindlimbs similar to arm and leg coordination in humans (4), which is unlike the lateral sequence seen in nonprimate mammal locomotion.
Bipedalism and the activity of the upper limbs share similar characteristics in primates and humans. Bipedalism in great apes is observed to be related to the foraging advantages in fruit trees gained with the upright posture (11). For example, although bonobos are habitual quadrupeds, they also engage in bipedal locomotion, both on terrestrial and in arboreal substrates. When their bipedal, quadrupedal, and even tripedal walking was contrasted in terms of kinematics and dynamics, the differences were very subtle, suggesting agreat overlap between the many locomotor modes in bonobos and that the required polyvalence is reflected in their anatomy (5).
It is theorized by Gebo that "positional behavior from early hominoids to hominids seems to have begun with an arboreal quadrupedal-climbing phase and proceeded through an orthograde, brachiating, forelimb-suspensory phase, which was in turn followed by arboreal and terrestrial quadrupedal phases before the advent of hominid bipedality" (11). Recent analyses of walking energetics and biomechanics for adult chimpanzees and humans provides more support to the long-standing hypothesis that bipedalism reduced the energy cost of walking compared with our ape-like ancestors (28).
WHY ARE THERE ARM-TO-LEG LINKAGES IN BIPEDAL HUMANS?
This question has been very difficult to address and is almost impossible to answer definitively. However, recent work related to the performance of bipedal locomotion in apes, monkeys, chimpanzees, and orangutans has provided new insight into the acquisition of bipedal locomotion in monkeys. Of particular interest, some new theories suggest a strong relation with the use of forelimbs, which has special implications for the arm and leg coordination issue in humans (Fig. 2). In physical anthropology, it is accepted that the divergence between hominids and our closest cousins, the chimpanzees, occurred between 5 and 7 million yr ago. The famous Laetoli footprints near Olduvai Gorge in Tanzania are dated to approximately 3.7 million yr ago, thus providing fossil evidence for bipedal locomotion within the past 4millionyr. These footprints are important because there are no concomitant knuckle-walking impressions suggesting some skill in bipedal walking. Recently, new analysis of fossil records of Oreopithecus bambolii suggests bipedal activity as early as 7-9 million yr ago (18). In sum, it is commonly accepted that there has been routine bipedal activity in primates for at least the past 4-6 million yr.
A dominant theory of how bipedal locomotion emerged was based on the concept of a survival advantage on the African savanna (see summary in (12)). That is, the ability to stand up and walk on the hindlimbs would provide an advantage to be able to view, intercept, avoid, or select predators, prey, and foraging items. A more recent theory that has gained some attention is that bipedal locomotor behavior in the chimpanzee and orangutan arose out of arboreal foraging behavior (29). When these primates seek fruit while climbing horizontally on branches, they frequently stand up and grasp a branch for stability. The more slender distal branches offer less support, reinforcing the need to seek stability by grasping a branch. Interestingly, this now leads to a switch in the coupling between the limbs such that one arm is used for support while the other arm is used for gathering. This explanation of the acquisition of bipedal locomotor behavior in our closest primate relations makes for an interesting parallel with human infant development where upright standing and locomotion is acquired (15). Both behaviors are focused on the exploring of novel environments. Hence, common environmental cues may beat play for both human developmental acquisition of bipedalism as well as the exploitation of bipedal locomotion in an evolutionary context. An interesting observation that can be obtained by a quick visit to any playground is that we humans have a very strong desire to climb. Monkey bars and climbing apparatus figure prominently in playgrounds. Niemitz (21) has commented that "It seems to be a trait of human behavioral genetics that Homo sapiens goes through an ontogenetic stage when climbing is an important and much liked part of the locomotor repertoire." The adaptive value of climbing - or arboreal walking - in humans may seem abstract in the urban environment. However, the ubiquitous nature of climbing and arboreal walking behaviors across primates is thought provoking. This also provides further context for the sensory linkage between arms and legs previously described for interlimb reflexes inhumans.
Some obvious biomechanical and functional differences exist between bipedal and quadrupedal gait. In bipedal locomotion, the center of mass is relatively high and balanced on only two legs, making the role of each leg critical. Also, during bipedal gait, the arms are not essential to the production of gait and can perform independent skilled hand movements. Despite these differences, the persistent preservation of the neuronal connections between rhythmic arm and leg movement may be related to the biomechanics of upright locomotion. It is possible that the use of arms for quadrupedal climbing evolved into use of the arms for offsetting interaction torques generated during upright bipedal terrestrial locomotion. As shown to the right in the simplified cartoon in Figure 3A, significant vertical whole body angular momentum rotation can be induced by the lower body motion during human walking and running (from the work of Hinrichs and colleagues cited in (7)). These effects are shown below in Figure 3B where an essential cancellation of total body angular momentum is seen to occur. That is, motion induced by leg movement is actively offset by upper body motion to minimize perturbations to running (and walking). This is not a passive process but rather an innate and active one requiring neuronal coordination. This is illustrated by the linked CPG networks shown schematically at the left of Figure 3A.
Interestingly, Witte et al. (30) used a mechanical analysis to show that stability about a vertical axis in human walking is maintained by body shape characteristics (such as breadth of hips and shoulders) and by swinging the arms out of phase with the swinging motion of the legs. From this standpoint, it reasons that mechanically advantageous movements of hindlimbs (legs) and forelimbs (arms) in bipedal humans are induced by essentially the same rhythm generator as in quadrupeds.
Before moving on to talk about the rehabilitative implications of these interactions, it is necessary to comment briefly on the limitations of the approach taken here. Our discussion has centered mainly on the role for spinal cord mechanisms in the coordination of arm and leg movement during locomotion and the essential similarities between humans and other animals. We freely admit that supraspinal regions contribute as well to this coordination. In fact, with reference to the first paragraph of this article, our human ability to do many other things with our arms (such as hold a coffee cup while walking to the office) speaks to our ability to superimpose voluntary supraspinal control on top of the basic spinal mechanisms of interlimb motor coordination. However, the specific detail of this form of coordination is beyond the scope of this brief review.
HOW CAN THESE LINKAGES BE EXPLOITED - WHAT ARE THE TRANSLATIONAL IMPLICATIONS FOR REHABILITATION?
Given the similarities between the organization of the motor systems and behaviors between nonhuman primates and humans, it has been proposed that nonhuman primates may provide a unique model for evaluating efficacy and safety of treatments for humans after neurotrauma, which would hasten the translation of interventions (3). In fact, it was demonstrated that the primate has the ability to rapidly regain locomotor performance and, to a lesser degree, fine foot motor skills, after a reduction in supraspinal control (4). The identification of the neural substrates mediating the rapid recovery of motor function may provide insight for the development of strategies to enhance functional recovery from neuromotor impairments in humans.
In the human, this question has been addressed by using various combinations of reduced or surrogate locomotion, including arm and leg stepping and cycling (32). Although recumbent stepping and cycling are similar to walking, an important difference is the extent of arm muscle activation and the direct mechanical coupling between the arms and legs. That is, the devices have handles and pedals that are mechanically coupled, allowing the arm movement to assist leg movement. This has been suggested to be of potential value in facilitating locomotor recovery after neurotrauma (9).
Recently, it was shown that rhythmic arm cycling could affect reflexes in leg muscles (10). Circuits active only during rhythmic movement (e.g., CPG activity) were suggested to cause this reflex attenuation and were speculated to represent a portion of the coordinated linkage between the arms and legs during locomotion (6,33). This suggests that normal coordination between the legs during walking is affected by activity in the arms (1). This has implications for recovery of walking after neurotrauma because the recovery of arm muscle coordination during rhythmic movement could assist with recovery of leg muscle activity. Behrman and Harkema (2) provided a description of case studies of locomotor retraining after spinal cord injury. They suggest that using the arms for postural and weight-bearing activity (e.g., on parallel bars or handrails) as is commonly applied in therapy may inhibit rhythmic stepping with the leg. In contrast, a normal reciprocating arm swing, such as found in natural walking, may facilitate stepping. They suggest that arm swing is an important component needed to help improve motor output for the legs during walking. Taken together, these observations support incorporating rhythmic arm movement paradigms for locomotor rehabilitation after neurotraumatic injury in humans. Ferris et al. (9) previously argued that, to harness interlimb neural coupling gait rehabilitation, therapy should incorporate simultaneous arm and leg rhythmic activity after neurotrauma. That is, neural commands related to the production of rhythmic arm movement could assist in accessing the neural circuitry underlying coupling between the arms and legs during locomotor retraining. In this way, rehabilitative interventions can move away from the concept of compensation for deficits and toward the attempt to tap into the intrinsic biology of the nervous system to facilitate motor relearning. Additional contributions from recent results suggest that cutaneous input from the hand may also help facilitate neural linkage between the arms and legs during locomotion (34). It is conceivable that the simultaneous arm and leg movement combined with cutaneous input from the skin of the hand linked to a stabilizing object may lead to facilitation of extensor muscle activity. However, this requires further exploration including a determination of any phase-dependent modulation across the full cycle of movement. Regardless, including specific use of the hands during the arm movement may be of importance in rehabilitation interventions. Elucidating these effects in a neurologically damaged population (e.g., after stroke or spinal cord injury) will be important to further refine effective rehabilitation strategies. Recently, Kawashima and colleagues (17) had people with incomplete cervical and complete thoracic spinal cord lesions perform locomotor-like arm and leg movements. In the incomplete cervical injury group, arm activity facilitated leg muscle activity, suggesting that neuronal activity related to the arm movement can enhance and "shape" motor output for the legs. They also go on to state that this "…neural interaction between upper and lower limb motions could be an underlying neural mechanism of human bipedal locomotion…" in keeping with the overall theme of this article.
SUMMARY AND CONCLUSIONS
In closing, the hypothesized conservation of elements of quadrupedal neural circuitry during bipedal locomotion has fundamental implications for the restoration and recovery of locomotor impairment occurring after stroke and spinal cord injury. This quadrupedal locomotor circuitry forms a base level for interlimb coordination that may be exploited in rehabilitation after neurotrauma to allow the arms to give the legs a helping hand during gait rehabilitation.
This study was supported by grants to E.P.Z. from the Natural Sciences and Engineering Council of Canada (NSERC), the Heart and Stroke Foundation of Canada (British Columbia and Yukon), and the Michael Smith Foundation for Health Research. S.R.H. was supported by fellowships from the Heart and Stroke Foundation of Canada (British Columbia and Yukon) and the Michael Smith Foundation for Health Research.
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