Goal-dependent tuning of muscle spindle receptors during movement preparation

AbstractVoluntary movements are believed to be advantageously prepared before they are executed, but the neural mechanisms at work have been unclear. For example, there are no overt changes in skeletal muscle activity during movement preparation. Here, using a delayed-reach manual task, we demonstrate a decrease in the firing rate of human muscle afferents (primary spindles) when preparing stretch rather than shortening of the spindle-bearing muscle. This goal-dependent modulation of proprioceptors begun early after target onset but was markedly stronger at the latter parts of the preparatory period. In two additional experiments, whole-arm perturbations during reach preparation revealed a congruent modulation of stretch reflex gains of shoulder and upper arm muscles. Our study shows that movement preparation can involve sensory elements of the peripheral nervous system. We suggest that central preparatory activity can also reflect sensory control, and preparatory tuning of muscle spindle mechanoreceptors is a component of planned reaching movements.

Download Full-text

Goal-dependent tuning of muscle spindle receptors during movement preparation

Science Advances ◽

10.1126/sciadv.abe0401 ◽

2021 ◽

Vol 7 (9) ◽

pp. eabe0401

Author(s):

Stylianos Papaioannou ◽

Michael Dimitriou

Keyword(s):

Muscle Spindle ◽

Muscle Force ◽

Muscle Stiffness ◽

Neural Mechanisms ◽

Manual Task ◽

Muscle Afferent ◽

Preparatory Activity ◽

Arm Muscles ◽

Task Goals

Voluntary movements are believed to undergo preparation before they are executed. Preparatory activity can benefit reaction time and the quality of planned movements, but the neural mechanisms at work during preparation are unclear. For example, there are no overt changes in muscle force during preparation. Here, using an instructed-delay manual task, we demonstrate a decrease in human muscle afferent activity (primary spindles) when preparing to reach targets in directions associated with stretch of the spindle-bearing muscle. This goal-dependent modulation of proprioceptors began early after target onset but was markedly stronger at the latter parts of the preparatory period. Moreover, whole-arm perturbations during reach preparation revealed a modulation of stretch reflex gains (shoulder and upper arm muscles) that reflected the observed changes in spindle activity. We suggest that one function of central preparatory activity is to tune muscle stiffness according to task goals via the independent control of muscle spindle sensors.

Download Full-text

Classification of human muscle stretch receptor afferents: a Bayesian approach

Journal of Neurophysiology ◽

10.1152/jn.1990.63.6.1314 ◽

1990 ◽

Vol 63 (6) ◽

pp. 1314-1322 ◽

Cited By ~ 49

Author(s):

B. B. Edin ◽

A. B. Vallbo

Keyword(s):

Muscle Spindle ◽

Small Amplitude ◽

Discharge Rate ◽

Muscle Afferents ◽

Human Muscle ◽

Golgi Tendon Organ ◽

Bayesian Decision ◽

Prior Probabilities ◽

Tendon Organ

1. A sample of 124 human muscle afferents originating from the finger extensor muscles were recorded from the radial nerve in the upper arm. A method is described to formalize the classification of units in muscle spindle primary and secondary afferents and Golgi tendon organ afferents on the basis of a few, nonrigorous assumptions. The classification was based on experimental data that largely have been described in a series of previous papers, although some additional data were collected in the present study. 2. The units were subjected to five tests providing identification data: twitch contraction test, ramp-and-hold stretch, small-amplitude sinusoidal stretches superimposed on ramp stretch, stretch sensitization, and isometric contraction/relaxation. From these five tests the following eight response features were extracted: response to maximal isometric twitch contractions, type of stretch sensitization, correlation between discharge rate and contractile force, response to sudden isometric relaxation, presence or absence of an initial burst, deceleration response, prompt silencing at slow muscle shortening, and driving by small-amplitude sinusoidal stretches. 3. A Bayesian decision procedure was adopted to classify the units on the basis of the eight discriminators. As a first step, units were provisionally classified into muscle spindle primary and secondary afferents, and Golgi tendon organ afferents, by intuitively weighting their responses to the identification tests. Prior probabilities were estimated on the basis of the provisional classification. The eight response features were analyzed and tabulated for all afferents, and the likelihood functions of the tests were directly calculated on the basis of these data.(ABSTRACT TRUNCATED AT 250 WORDS)

Download Full-text

Dynamic response of human muscle spindle afferents to stretch

Journal of Neurophysiology ◽

10.1152/jn.1990.63.6.1297 ◽

1990 ◽

Vol 63 (6) ◽

pp. 1297-1306 ◽

Cited By ~ 114

Author(s):

B. B. Edin ◽

A. B. Vallbo

Keyword(s):

Dynamic Response ◽

Muscle Spindle ◽

Human Subjects ◽

Muscle Afferents ◽

Human Muscle ◽

Golgi Tendon Organ ◽

Muscle Spindle Afferents ◽

Partial Data ◽

Extensor Muscles ◽

Tendon Organ

1. One hundred and twenty-four muscle afferents from the finger extensor muscles were recorded from the radial nerve in human subjects. 2. The afferents were provisionally classified as muscle spindle primary (78/124) and secondary afferents (25/124), and Golgi tendon organ afferents (21/124), on the basis of their response to 1) maximal twitch contractions, 2) 20- and 50-Hz sinusoids superimposed on ramp-and-hold stretches, 3) stretch sensitization, and 4) isometric contractions and sudden relaxations. 3. Ramp-and-hold stretches at two velocities, 10 and 50 degrees/s, were applied to the appropriate metacarpophalangeal (MCP) joint while the parent muscle remained relaxed. For each unit three discrete parameters were assessed: the presence or absence of 1) an initial burst at the commencement of the ramp stretch, 2) a deceleration response at the beginning of the hold phase, and 3) a prompt silencing at muscle shortening. In addition, two kinds of dynamic indexes were calculated for 79 of the muscle spindle afferents. 4. Most spindle afferents responded readily to stretch, whereas the Golgi tendon organ afferents produced very poor stretch responses. All of them lacked a static response, whereas the dynamic response, when present at all, consisted of only a few impulses. 5. The dynamic index was higher for spindle primaries than for secondaries, and this difference was statistically significant although the distribution was unimodal for spindle afferents as a group. Hence, this parameter was a poor discriminator. 6. Initial bursts, deceleration responses, and silences during imposed shortening were more common in spindle primaries than in secondaries. The differences were significant in all these respects. 7. The three discrete parameters were statistically pairwise independent for the spindle afferents, justifying the combination of the three into a useful battery for discrimination between primary and secondary spindle afferents and the use of this battery as a partial data base for a probability approach towards a solid classification of human muscle afferents.

Download Full-text