ReviewMuscle proprioceptive feedback and spinal networks
Introduction
“Can sense be made of spinal interneuron circuits?” [247]. Already two decades ago, Loeb [214] wrote: “Those whose experiments have forced us to confront the ‘embarassment of riches’ in the workings of the spinal cord must ask whether it is useful to continue to collect yet more inexplicable data. Those who believed the spinal cord and peripheral motor plant to be well-understood and thus turned their attentions to higher centers of motor planning and coordination (e.g. cerebral cortex and cerebellum) now find that their edifices are built upon ‘the shifting sands of spinal segmental circuitry’ (Stuart, D.G., unpublished)” (p. 111). Addressing the ‘sense’ of the spinal Renshaw cell (intercalated in the inhibitory circuit from motor axon collaterals to ventral horn neurons and named in honor of its discoverer: Renshaw [308]), Zev Rymer felt that, “given the simplicity of the circuit, and its direct proximity to motor outflow, our failure to clarify the function of the Renshaw neuron is an embarassment, and does not generate confidence that computational approaches used to describe complex neural circuits will yield useful answers” (cited in ref. [391], p. 520). Does our quest for understanding spinal circuits end in embarassment? Yes and no, as discussed below.
As requested by the editor, this review will revolve primarily around segmental feedback systems established by muscle spindle and Golgi tendon organ afferents (muscle proprioceptive1 afferents), as well as spinal recurrent inhibition via Renshaw cells. At first glimpse, this association appears somewhat arbitrary, but it has a long tradition. The discussion will thus focus on spinal circuits, but since segments neither in the spinal cord nor in the body and limbs are isolated, the view will at times have to fly out beyond the narrow confines of spinal circuits in order to integrate them into wider concepts. The literature on these issues is immense, and the selection is necessarily restrictive and subjective.
Section snippets
Organization of scratch reflexes
In the 19th and first half of the 20th century, the spinal cord was considered, besides as a conductive structure, primarily as a reflex machine. “The application of the term reflex to such acts seems to have been made first by Descartes (1649), on the analogy of the reflection of light, the sensory effect in these cases being reflected back, so to speak, as a motor effect” ([150], p. 141). The optic analogy suggests a deceiving simplicity, which illusion appears to have survived until today.
Rhythmogenesis
In order to produce the rhythmic scratch-reflex component as well as other rhythmic movements (e.g., locomotion, mastication, respiration), the CNS makes use of complex networks of neurons, which are generally called ‘central pattern generators’ (CPGs) [185]. While in principle they may produce rhythmic motoneuron activities without sensory feedback and signals descending from supraspinal structures, these inputs shape the timing and magnitude of motoneuron activities, and their processing is
Generation of upright body posture
During upright stance of animals suspending their body above the ground by means of legs, the controlling neural system should meet the following general requirements:
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Anti-gravity function [236]:
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Generation of upward thrust by provision of muscle tone in anti-gravity muscles.
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Balance. Under stationary conditions of upright stance, the projection of the body's center of mass must fall within the base of support.
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Coordination of proper muscle torques across the series of limb, trunk and neck joints.
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Muscle proprioceptive feedback and recurrent inhibition in action
So far, the discussion has concentrated on stationary stance conditions. Now the question arises as to the behavior and role of muscle proprioceptive feedback and recurrent inhibition in dynamic movements.
Stabilization of motor output
In the mathematical literature in general and in biological motor control in particular, ‘stability’ is not defined unanimously. Nor does it represent a value per se in the sense that the nervous system should immediately act to oppose any small perturbation at the cost of maneuverability [138]. Under some conditions, however, some variables must be stabilized against internal and external perturbations, with mechanisms to compensate for these perturbations. For example, external perturbations
Compensation for muscle fatigue
Muscle fatigue is a severe internal disturbance of the peripheral mechanical apparatus, which must be taken care of by the nervous system while generating posture and movement.
Muscle fatigue becomes manifest as “… any reduction in the force generating capacity of the total neuromuscular system regardless of the force required in any given situation” ([27], p. 691). This decline involves processes at all levels of the motor pathway from the brain to skeletal muscle [90], [91], [111]. Processes
Summary and comments
Decades of experimental work on spinal sensory-motor systems have led to some general operational ideas or ‘principles’ [164], [165], which can also be considered as guidelines for future research.
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Flexibility. Functionally, spinal networks are anything but fixed and prewired so as to yield, for instance, stereotypic reflexes. Thus, reflexes can be adjusted to the type, intensity and site of action of stimuli and their context [153], [154], [165].
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Fractionation. Spinal neurons are divided into
‘Global roles’ of proprioceptive afferents
Multi-joint systems pose severe problems. First, the positions and movements of different joints need to be coordinated, which leads into the issue of synergies and their neuromuscular organization (this main section). Second, more generally and abstractly, spatial relations of body parts require a central representation commonly referred to as body schema, which will be discussed in the context of postural adjustments (Section 10). Third, movements of coupled body segments depend on each other
Postural maintenance and adjustments
Upright posture of animals standing on legs is a shaky condition, particularly in two-legged animals, such as humans and birds. It is always jeopardized by internal and external influences, permanently by gravity, and thus necessitates continuous stabilization. Despite its name, stabilization of static equilibrium is a dynamic process because the body is always in motion and keeping the center of gravity above the support base therefore requires continuous, more or less large postural
Proprioceptive feedback in intersegmental interaction dynamics
Since body segments are movably coupled at the joints, they exchange potential and kinetic energy throughout a movement, with energy flowing into or out of the segments. This has at least two implications. (i) An external perturbation impinging on one segment will also act on others. (ii) The actions of skeletal muscles on movements are often derived from their anatomical sites of origin and insertion. This notion is oversimplified and essentially wrong, however. The force a muscle generates
Plasticity, adaptability and learning
Obviously, the CNS must adapt its actions to changing conditions of the environment, including its own body, and learn from their effects, at very different levels of organization and time scales. This requires its neuronal networks, including reflex pathways, to be plastic rather than rigid. In a narrow behavioral sense, motor learning implies the acquisition of new behaviors or skills by practice [79]. But the term is often used with wider connotations including processes and mechanisms at
Transformations revisited
“The spinal cord circuitry is in fact capable of solving some of the most complex problems in motor control and, in that sense, spinal mechanisms are much more sophisticated than many neuroscientists give them credit for” ([295], p. 269). Specifically, the vertebrate spinal cord is able to solve, at least to some degree, (i) the degrees-of-freedom problem, (ii) the problem of complex spatial sensory-motor transformations, and (iii) the inverse dynamics problem [295].
While, at a global level,
Final comments
“Can sense be made of spinal interneuron circuits?” [247]. Yes and no, depending on what is meant by ‘making sense’. Most investigators would probably agree that making sense is closely related to understanding the ‘function’ or ‘role’ of the nervous system or its parts in normal animal behaviors. Of course, sense and understanding depend, besides on our mental capacities, investigative means and concepts employed to penetrate reality, on the level of organization: whole organism, macroscopic
Conflict of interest
None.
Acknowledgements
I am very grateful for encouraging comments and helpful suggestions to Drs. A. Moschovakis, T.R. Nichols, R.E. Poppele, S. Roatta, M. Schieppati, and D.G. Stuart.
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