خواسته های عصبی و عضلانی از راه رفتن پا: یک تجزیه و تحلیل شبیه سازی دینامیکی رو به جلو

Toe walking is a gait deviation with multiple etiologies and often associated with premature and prolonged ankle plantar flexor electromyographic activity. The goal of this study was to use a detailed musculoskeletal model and forward dynamical simulations that emulate able-bodied toe and heel-toe walking to understand why, despite an increase in muscle activity in the ankle plantar flexors during toe walking, the internal ankle joint moment decreases relative to heel-toe walking. The simulations were analyzed to assess the force generating capacity of the plantar flexors by examining each muscle's contractile state (i.e., the muscle fiber length, velocity and activation). Consistent with experimental measurements, the simulation data showed that despite a 122% increase in soleus muscle activity and a 76% increase in gastrocnemius activity, the peak internal ankle moment in late stance decreased. The decrease was attributed to non-optimal contractile conditions for the plantar flexors (primarily the force–length relationship) that reduced their ability to generate force. As a result, greater muscle activity is needed during toe walking to produce a given muscle force level. In addition, toe walking requires greater sustained plantar flexor force and moment generation during stance. Thus, even though toe walking requires lower peak plantar flexor forces that might suggest a compensatory advantage for those with plantar flexor weakness, greater neuromuscular demand is placed on those muscles. Therefore, medical decisions concerning whether to reduce equinus should consider not only the impact on the ankle moment, but also the expected change to the plantar flexor's force generating capacity.

Toe walking is a gait deviation with multiple etiologies ranging from cerebral palsy to traumatic brain injury. It is often associated with premature and prolonged ankle plantar flexor electromyographic (EMG) activity (e.g., Colborne et al., 1994; Kalen et al., 1986), spasticity (e.g., Cahan et al., 1989; Perry et al., 1974) and contractures (e.g., Kelly et al., 1997; Stricker and Angulo, 1998). The increased plantar flexion posture can compromise walking stability and often results in decreased stride length and walking speed (Cahan et al., 1989; Davids et al., 1999; Hicks et al., 1988). Recently, it has been proposed that toe walking provides a compensatory advantage over conventional heel-toe walking (Hampton et al., 2003; Kerrigan et al., 2000). Kerrigan et al. (2000) performed an inverse dynamics-based analysis of able-bodied subjects during heel-toe and toe walking and observed a significant decrease in the peak internal ankle plantar flexor moment and power generated in terminal stance and pre-swing during toe walking. They concluded that toe walking may provide a benefit for those with upper motor neuron injury and distal lower extremity weakness by requiring lower ankle plantar flexor strength. Similarly, Hampton et al. (2003) performed a quasi-static analysis of the foot and tibia using data recorded from able-bodied subjects emulating toe walking postures of individuals with cerebral palsy. Their results showed that the increased equinus posture results in reduced plantar flexor force requirements. The reduced plantar flexor force (primarily from the gastrocnemius and soleus) was attributed to the closer proximity of the resultant ground reaction force vector to the ankle joint center with greater angles of plantar flexion. Similar to Kerrigan et al. (2000), they concluded that equinus walking is most likely a compensatory strategy for plantar flexor weakness. While these studies noted a reduction in the plantar flexor force requirements during toe walking, Perry et al. (2003) demonstrated using fine wire electromyography that plantar flexor muscle activity during toe walking is greatly increased in late stance despite a reduced net plantar flexor moment. They hypothesized that the dichotomy between increased muscle activity and decreased joint moment was due to a reduction in force generating capacity of the ankle muscles because of greater plantar flexion angles during toe walking. Thus, although the peak plantar flexor force required during toe walking may be lower, the neuromuscular demand placed on the plantar flexors appears to be greater. The isometric moment generation of the plantar flexors decreases with increasing plantar flexion angles (e.g., Gravel et al., 1988; Miyamoto and Oda, 2003; Nistor et al., 1982; Sale et al., 1982), despite an increase in the moment arm of the gastrocnemius and soleus about the ankle joint with increasing plantar flexion angles (Rugg et al., 1990). The decrease in moment output is attributed to the muscles operating at non-optimal lengths on the muscle fiber force–length relationship. Thus, the increased ankle plantar flexion angle during toe walking likely reduces the force-generating capacity of the muscles. In addition, walking contains periods of both shortening and lengthening contractions of the plantar flexor muscles. Therefore, the muscle force generating capacity during walking could be impacted by both changes in fiber length as well as velocity. The poor contractile conditions associated with increased plantar flexion angles was recently highlighted in a modeling and simulation study showing that as ankle plantar flexion increases with walking speed, the force generating capacity of the plantar flexors becomes increasingly impaired (Neptune and Sasaki, 2005). The goal of the present study was to explicitly test the hypothesis that greater angles of plantar flexion during toe walking are associated with a lower force generating capacity of the ankle plantar flexors compared to the normal posture in heel-toe gait. A detailed musculoskeletal model and forward dynamical simulations of able-bodied toe and heel-toe walking were developed to assess the force generating capacity of the plantar flexors by examining each muscle's contractile state. Specifically, we examined the muscle fiber length, velocity and activation relationships during toe and heel-toe walking to assess whether toe walking requires greater neuromuscular effort.

Consistent with our previous simulation analyses (e.g., Neptune et al., 2001; Neptune and Sasaki, 2005), the dynamic optimization was able to identify muscle excitation patterns such that the toe and heel-toe walking simulations closely emulated the human subject body segment kinematic, ground reaction force and internal joint moment data. The walking speeds were 1.16 and 1.14 m/s for toe and heel-toe walking simulations, respectively. Of particular importance to the present study was the ability of the simulation to closely match the human subject ankle joint kinematics and internal moment profiles. The simulation was able to reproduce these quantities within ±2 standard deviations of the experimental data (Fig. 4). In both simulations, the timing of the plantar flexor activity compared well with the experimental EMG data (Fig. 4). Despite a 122% increase in soleus (SOL) muscle activity during toe walking, the corresponding average SOL muscle force during stance decreased by 19% relative to heel-toe walking (Fig. 5). The gastrocnemius (GAS) muscle activity increased 76% during toe walking, however, this only resulted in a 37% increase in the average GAS muscle force (Fig. 5). The magnitude of the muscle forces was consistent with the net internal ankle joint moment. Despite the increase in plantar flexor activity during toe walking (Fig. 5), the peak ankle moment during late stance decreased slightly (Fig. 6). This reduction in the simulation ankle moment, despite the greater muscle activity, was attributed to a poor contractile state during toe walking, primarily due to the muscles operating at non-optimal muscle fiber lengths when the ankle was in greater plantar flexion (Fig. 4). The mean SOL fiber length normalized to its optimal fiber length during its active region in stance was 0.55 and 0.89 during toe and heel-toe walking, respectively (Fig. 7A). Similarly, the mean values for GAS were 0.59 and 0.90, respectively (Fig. 7A). Thus, both muscles were operating near the onset of the ascending limb of the force–length relationship (Fig. 3A), which greatly reduced their ability to generate force. In contrast, the mean fiber velocities were at low levels and similar in magnitude between the two walking tasks (Fig. 7B). Thus, the force–length relationship was the dominant intrinsic muscle property that decreased the force generating capacity of the plantar flexors during toe walking. In addition to the greater intensity and duration of muscle excitation required for toe walking, maintaining the plantar flexed posture throughout stance required a 65% increase in the mean internal ankle moment during stance (Fig. 6: 1.11 and 0.68 N -m/kg for toe and heel-toe walking, respectively).