Patterned control of human locomotion

Abstract

There is much experimental evidence for the existence of biomechanical constraints which simplify the problem of control of multi-segment movements. In addition, it has been hypothesized that movements are controlled using a small set of basic temporal components or activation patterns, shared by several different muscles and reflecting global kinematic and kinetic goals. Here we review recent studies on human locomotion showing that muscle activity is accounted for by a combination of few basic patterns, each one timed at a different phase of the gait cycle. Similar patterns are involved in walking and running at different speeds, walking forwards or backwards, and walking under different loading conditions. The corresponding weights of distribution to different muscles may change as a function of the condition, allowing highly flexible control. Biomechanical correlates of each activation pattern have been described, leading to the hypothesis that the co-ordination of limb and body segments arises from the coupling of neural oscillators between each other and with limb mechanical oscillators. Muscle activations need only intervene during limited time epochs to force intrinsic oscillations of the system when energy is lost.

Figure 1. Schematic of patterned control

Simulated example of muscle activity profiles as weighted sum of three basic temporal patterns. A given pattern and its associated weights of distribution to all muscles represent a control module. The outputs of the first (green), second (blue) and third (red) modules are summed together to generate overall muscle activation (black envelope) according to the equation: m_i(t) = ∑_jp_j(t)w_ij, where m is muscle activation, p is pattern and w is weight.

Figure 2. Basic patterns and effect of walking speed

A, basic patterns obtained by non-negative matrix factorization of averaged (across steps) rectified EMG profiles of 16 unilateral leg muscles (see list in Fig. 3A) in 10 walking subjects. Patterns are plotted versus normalized gait cycle. VAF cumulative variance accounted for by all patterns. B, upper plot: changes in the relative duration of the stance phase with speed. Lower plot: phase lag required to provide the best fit between each pattern and the pattern determined from the 5 km h⁻¹ data. B is modified from Ivanenko et al. 2004.

Figure 3. Forward versus backward locomotion

Patterns and weights in forward (A) and backward (B) walk at 5 km h⁻¹ on treadmill. Notice that the patterns are similar between forward and backward locomotion, but the weights are drastically different.

Figure 4. Effect of loading and unloading

In each row, a basic pattern is plotted versus normalized gait cycle (as in Figs 2 and 3), and scaled in amplitude for the indicated muscles and loading conditions (see legend). For each condition, all muscles within a module received the same activation timing and waveform, but the magnitude was allowed to vary. Both timing and magnitude were allowed to vary between conditions. GMAX, gluteus maximus; GMED, gluteus medius; VAS, 3-components vastus (medialis, lateralis, intermedius); RF, rectus femoris; HAM, hamstrings; BFsh, short head of biceps femoris; MGAS, medial gastrocnemius; SOL, soleus; TA, tibialis anterior. Modified from McGowan et al. (2010) with permission from Elsevier.

Figure 5. Contributions of basic patterns to walking biomechanics

Contribution of different patterns (modules) to the walking sub-tasks of body support, forward propulsion and leg swing. Early stance (15% of gait cycle), late stance (45%), early swing (70%) and late swing (85%) are shown. Arrows departing from the COM denote the resultant module contributions to the horizontal and vertical ground reaction forces that accelerate the COM providing body support and forward propulsion. Net energy flow by each module to the trunk or leg is denoted by a + or – for energy increases or decreases, respectively. Muscle abbreviations are as in Fig. 4. Modified from Neptune et al. (2009) with permission from Elsevier.

Figure 6. Mechanical oscillations during walking

A, schematic trajectory of COM during a few consecutive steps. Arrows denote COM velocity before and after heel contact. Notice that p₁ and p₄ timing coincides with the redirection of COM velocity. B, planar co-variance of thigh elevation angle versus shank and foot angles identifies counter-clockwise loops, with heel contact and toe-off at the top and bottom. Each coloured trace in both A and B denotes the trajectory segment over which the indicated pattern is active.

Figure 7. Schematics of neural substrates

A, multi-layered organization of rhythm and patterns generators in the spinal cord under descending and sensory influence. B, Matsuoka neural oscillators. See text for explanation.