Elsevier

Current Opinion in Neurobiology

Volume 33, August 2015, Pages 156-165
Current Opinion in Neurobiology

Motor primitives  new data and future questions

https://doi.org/10.1016/j.conb.2015.04.004Get rights and content

Highlights

  • Motor primitive analyses can capture kinematic and muscle level organization of movement across reflex, locomotor and novel skilled tasks.

  • Kinematic structure and a compositional system of motor primitives are found across many species ranging from octopus through frog to man.

  • Kinetic/muscle synergy types of motor primitives are found in limb use in all tetrapod vertebrates examined.

  • Representation of ethologically important motor primitives has been reported for reaching and grasping tasks in primates.

  • Data supporting collections of motor primitives embedded at a low level in spinal cord now derive from a range of methods and species.

Motor primitives allow integration across scales in the motor system and may link movement construction and circuit organization. This review examines support for primitives, and new data relating primitives to concrete circuit elements across species. Both kinematic motor primitives and muscle synergy/kinetic motor primitives are reviewed. Motor primitives allow a modular hierarchy that may be re-used by volitional systems in novel ways. They can provide a developmental bootstrap for ethologically important actions. Collections of primitives somewhat constrain motor acts, but at the same time sets of primitives facilitate the rapid construction of these constrained actions, and can allow use of simpler controls. Novel motor skill likely requires augmentation to transcend the constraints present in initial collections of low level motor primitives. The benefits and limitations of motor primitives and the recognized knowledge gaps and needs for future research are briefly discussed.

Introduction

Motor Primitives can be controversial. What is a ‘primitive’? The Free Dictionary online (http://www.thefreedictionary.com/primitive) states: 1. Not derived from something else; primary or basic. 2. a. Of or relating to an earliest or original stage or state; primeval. b. Being little evolved from an early ancestral type. 3. Characterized by simplicity or crudity. These definitions are close to what many of us consider ‘Motor Primitives’ to be in neuroscience, i.e., fundamental building blocks for constructing motion. Motor primitives (MPs) are thus defined here to be compositional elements for movement construction. Assuming more complex motion arises from rearranging and combining MPs, then a subset of fundamental motor primitives should be available to organize initial movements very early in development, and thereby contribute to the ontogenetic and adult construction of more complex motor acts, in one or more ways.

Compositional elements for movement could have various forms. Motor acts comprise overall kinematics, together with force interactions with the environment, and the underlying body kinetics, and regulation of impedance. These in turn depend on patterns of muscle activation and control. At what level should we look for compositional MPs as motor neuroscientist? Different authors have considered MPs at several levels. MPs have been defined as kinematic elements (i.e., patterns of motion without regard to force or mass, e.g., strokes [1, 2, 3•] or cycles [4, 5]), or as kinetic elements (force-based, e.g., viscoelastic force-field primitives [6, 7, 8, 9] and their associated muscle synergies [9, 10, 11]), or as neural drive circuits [12]. Because the nervous system appears to organize both the executed motion as well as prepare the contingent acts and corrections required for any common or unexpected perturbations in any complex body motion, it follows that the most fundamental MPs need to be useful as compositional elements in each of these contexts, i.e., the fundamental MPs must be adequate building blocks to rapidly construct the kinematic, kinetic, impedance and contingent response aspects of a complex movement. Our current computational understanding of motor control likely has a place for both kinematic and kinetic elements [3•, 13, 14, 15]. However, reconciling the frameworks of kinematic MPs and kinetic/synergy MPs into a unified compositional scheme remains difficult. Explorations that enrich our understanding of movement in important ways continue in both areas as described below. Here I take the kinetic MPs as fundamental building blocks, and take kinematic MPs as more derived, according to the mechanical relations between them, but a satisfying unification of the two in motor neuroscience is eventually needed.

Section snippets

Evidence for kinematic movement primitives

Support for kinematic MPs derives from several methods. Primarily, researchers seek building blocks in complex kinematic patterns, decomposing motor acts at the kinematics level into their constituent elements. Various statistical techniques are available, each with pros and cons, to accomplish this task and break motion patterns into component elements. Early segmentation of kinematics by Viviani and Terzuolo, and by Flash and Hogan [2] has been elaborated today in several further ways.

Evidence for force-field motor primitives and spinal muscle synergies

Support for visco-elastic force fields as kinetic MPs and for their associated muscle synergies as MPs is strong (Figure 1, MP2). These two descriptions (force-field unit and muscle synergy) are equivalent to one another and largely interchangeable (see Figure 2, for more details). Support derives from physiological perturbations, neural recordings, statistical decomposition techniques in animal and human model system data, and more recently from molecular genetics methods and manipulations.

Circuit foundations of motor primitives

If MPs reflect an organizational principle in movement construction, we should expect the MP picture to give insight into the underlying circuits, e.g., spinal system architectures, in addition to forming motor pattern and biomechanical building blocks. Strong predictions of an MP framework are that the underlying neural circuitry should involve interneurons assembling the synergies and driving them as units. The simplest conceptions of these are as simple premotor projection neurons. In the

Computational frameworks for motor primitives

Both kinematic and force-field/muscle synergy MPs are currently viewed as rooted in some kind of optimization of movement or an approximation of it [2, 15, 23, 24]. The form of kinematic strokes in movement (i.e., MP1, Figure 1) have variously been attributed to the central nervous system (CNS) minimizing jerk, torque change, muscular effort or some weighted balance of these [2, 15, 23, 24]. Kinematic MPs are seen in a range of animal forms from soft-bodied muscular hydrostat effectors, to

Development, skill and plasticity in relation to Motor Primitives in humans

The concept of MPs raises a range of questions in human development. What collections of MPs are available in man, based on our current understanding, and do they constrain our options for human movement? Do skilled biped primates still continue to utilize the ‘built-in’ MPs seen in other specie? Are human and primate MPs constructed de novo in novel tasks, or for bipedal locomotion? Do neocortical representations replace or incorporate the evolutionarily older systems in skilled novel

Conclusions  Major issues for the future

Motor Primitives at a low level in the CNS can provide an animal with initial simplified control of movement, and can bootstrap development of movement using information captured and ‘baked in’ by many prior generations of evolutionary selection pressure, forming modularity that is closely matched to the biomechanics and standard movement repertoire. MPs may thereby almost immediately provide near optimal patterns of muscle activation in some species with high early motor demands. MPs also form

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgments

Support from NIH NS072651, NS054894, NSF IIS 0827684 and the Craig Neilsen Foundation. Drs. Kim Dougherty, Ole Kiehn, and Brian Clark made very helpful comments on earlier versions of the manuscript.

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