Motor primitives and synergies in the spinal cord and after injury--the current state of play

Abstract

Modular pattern generator elements, also known as burst synergies or motor primitives, have become a useful and important way of describing motor behavior, albeit controversial. It is suggested that these synergy elements may constitute part of the pattern-shaping layers of a McCrea/Rybak two-layer pattern generator, as well as being used in other ways in the spinal cord. The data supporting modular synergies range across species including humans and encompass motor pattern analyses and neural recordings. Recently, synergy persistence and changes following clinical trauma have been presented. These new data underscore the importance of understanding the modular structure of motor behaviors and the underlying circuitry to best provide principled therapies and to understand phenomena reported in the clinic. We discuss the evidence and different viewpoints on modularity, the neural underpinnings identified thus far, and possible critical issues for the future of this area.

Figure 1

Simulating hindlimb wiping with a detailed model of the spinal primitives. (A) The 13 hindlimb muscles forming the biomechanical model are shown as red lines. Colored arrows mark the force directions of the three force primitives at a fixed limb position during the isometric wiping response: KF (knee flexor primitive), light purple; HE (hip extensor primitive), green; HF (hip flexor primitive), dark purple. (B) The framework used to simulate wiping (left to right): each primitive had a time-course generator, representing the premotor drive burst, which output a normalized waveform (peak = 1.0) at time τ. The variable A scaled this waveform, which was then distributed to each of the muscles within the primitive. Each muscle had a muscle-specific variable C that scaled the excitation wave form. The synergy muscle groups generate contractile forces MF that are transmitted through the limb to produce anisometric endpoint force (at one position) or force field FF (when forces are measured across a range of positions). Normalized force fields produced by each primitive are shown in the far right. When the model limb is freed to move, MFs drive the motion of the model. MF values are in turn regulated by the limb motion (i.e., the force–velocity and force–length properties of muscle and stress–strain properties of in series connective tissue alter MF forces). In this version model, sensory feedback from muscles potentially regulate τ A or C. ILf, iliofibularis; STd, semitendinosus dorsal branch; STv, semitendinosus ventral branch; ILm, iliacus median; Ile, iliacus externus; ILi, iliacus internus; GL, gluteus; SA, sartorius; TA, tibialis anticus; SM, semimembranosus; GR, gracilis; ADd, adductor dorsal; ADv, sdductor ventral; QF, quadratus femoris; PL, peroneus longus. Reproduced from Ref. , with permission.

Figure 2

Examining reproducibility of frog primitives. Stability of muscle proportionality ratios in the six main primitives are observed across frogs and across behaviors. The action of the spinal cord across the tested behaviors was to recruit the muscles in fixed ratios and thereby couple muscles so as to generate specific force-field primitives and associated preflex responses. Reflex actions (i.e., feedback effects) modulated these primitives, not individual muscles (see Ref. 53), and thus acted on their component muscles as groups. HF, hip flexor synergy. Muscle Abbrev (nomenclature of Ecker, with equivalent Abbott and Lombard): VI, vastus internus (= iliacus internus); VE, vastus externus (= iliacus externus); BI, biceps (= Iliofibularis); AD, adductor magnus; SA, sartorius; RA, rectus anticus (= quadratus femoris); GL, gluteus. Reproduced from Ref. , with permission.

Figure 3

Simulation results using a framework of primitives. Simulating wiping forces and kinematics with the primitive framework and model frog. (A) Model structure. (B) Activation of muscles as synergies. (C) The isometric force pattern produced by the model frog (solid lines) closely matched the force pattern recorded experimentally (dotted lines). (D) After making minor adjustments to the isometric motor pattern (amplitude scaling the ensemble down slightly) the model frog also reproduced the free limb kinematics of the experimental frog. Without downscaling the forces were too strong, indicating potential feedback adjustment in isometric conditions. The top row shows hip and knee angles. The bottom row shows ankle velocity. Dashed line marks the time of target limb contact in the real frog. The gray area (PM) represents the 40-ms premovement period between EMG onset and motion onset that is observed in real frogs.