Human motor control consequences of thixotropic changes in muscular short-range stiffness

Abstract

1. The primary aim of the present study was to explore whether in healthy subjects the muscle contractions required for unrestrained voluntary wrist dorsiflexions are adjusted in strength to thixotropy-dependent variations in the short-range stiffness encountered in measurements of passive torque resistance to imposed wrist dorsiflexions. 2. After a period of rest, only the first movement in a series of passive wrist dorsiflexions of moderate amplitude exhibited clear signs of short-range stiffness in the torque response. During analogous types of voluntary movements, the extensor EMG during the first movement after rest showed a steep initial rise of activity, which apparently served to compensate for the short-range stiffness. 3. The passive torque resistance to minute repetitive wrist dorsiflexions (within the range of short-range stiffness) was markedly reduced after various types of mechanical agitation. During analogous low-amplitude voluntary wrist dorsiflexions the extensor EMG signals were weaker after than before agitation. 4. Mechanical agitation also led to enhancement of passive dorsiflexion movements induced by weak constant torque pulses. In an analogous way, the movement-generating capacity of weak voluntary extensor activations (as determined by EMG recordings) was greatly enhanced by mechanical agitation. 5. The signals from a force transducer probe pressed against the wrist flexor tendons--during passive wrist dorsiflexions--revealed short-range stiffness responses which highly resembled those observed in the torque measurements, suggesting that the latter to a large extent emanated from the stretched, relaxed flexor muscles. During repetitive stereotyped voluntary wrist dorsiflexions, a close correspondence was observed between the degree of short-range stiffness as sensed by the wrist flexor tension transducer and the strength of the initial extensor activation required for movement generation. 6. The results provide evidence that the central nervous system in its control of voluntary movements takes account of and compensates for the history-dependent degree of inherent short-range stiffness of the muscles antagonistic to the prime movers.

Figure 4. Aftereffects of stirring manoeuvres on the amplitude of passive wrist dorsiflexions induced by weak repetitive torque pulses (A) and on the amplitude of dorsiflexions actively generated by repetitive weak extensor contractions (B)

A, example of the Flap. manoeuvre causing a marked enhancement on the hand excursions induced by repetitive torque pulse applications. The two vertical dotted bars in the goniometer trace indicate the mean amplitude of three excursions induced by the torque pulses immediately before and after the Flap. maneouvre. B, example of a Flap. manoeuvre causing an equally marked enhancement of the movement-generating capacity of weak wrist extensor contractions. The two dotted bars in the goniometer trace indicate the mean amplitude of the excursions as in A. (In both A and B the goniometer amplifier was overloaded during the high amplitude Flap. manoeuvres.)

Figure 1. Torque responses to passive repetitive wrist dorsiflexions exceeding the limit for the short-range stiffness

A, with the subject relaxed (as confirmed by IEMG records) the torque responses to manually imposed repetitive wrist dorsiflexions are displayed as up-going deflexions from the zero torque baseline (dashed line). In the goniometer trace wrist dorsiflexions are displayed as up-going deflexions from a baseline (dashed line) assigned as the zero level and indicating the wrist resting position after the standard ‘pre-test’ conditioning manoeuvre described in Methods. B, X-Y plot of torque against wrist displacement for the three consecutive movements shown in A. The upper horizontal dashed line indicates the torque response to the first dorsiflexion at 2 deg and the horizontal middle dashed line indicates the corresponding response to the second movement (which in this particular recording also represents the zero torque level). The lower horizontal dashed line indicates the torque level at the onset of the second movement. The two vertical dotted bars (to the right) indicate the increase in torque resistance for the two movements over the first 2 deg, i.e. measurements used for quantification. Note that the torque responses to the second and the third movements are almost indistinguishable.

Figure 3. Passive compared to active repetitive wrist dorsiflexions of low enough amplitude to not exceed the limit for the short-range stiffness: effects of stirring manoeuvres

A, torque responses to passive repetitive low amplitude dorsiflexions induced before and after high-amplitude flapping hand movements (Flap.). The two vertical dotted bars in the torque trace indicate the mean torque response to three movements before and after the Flap. manoeuvre. B, strength of extensor contractions required for active repetitive dorsiflexions of similar low amplitude as the passive movements shown in A. The two vertical dotted bars in the extensor IEMG trace indicate the mean IEMG amplitude for three movements before and after a stirring manoeuvre consisting of mechanical vibration applied over the wrist flexor muscles (Vib.).

Figure 5. Wrist flexor tension responses as sensed by force transducer firmly pressed against the flexor tendons during passive wrist movements

A, flexor tension responses to passive repetitive wrist dorsiflexions of similar speed and amplitude to those illustrated in Fig. 1A. Note the extent to which the signals from the flexor force transducer resemble the torque responses in Fig. 1A. Dashed lines in tension traces show the tension base line (arbitrarily assigned to be zero force) without account being taken of the steady-state pressure exerted by the strain gauge probe against the flexor tendons. B, example of wrist flexor tension responses to passive repetitive wrist volarflexion movements. Note that in response to the first (and fourth) passive shortening movements (after periods of rest) the relaxed flexors exhibit a steep initial fall in tension followed by a less prominent decline, i.e. a response which is the reverse of that induced by passive repetitive dorsiflexions (cf. responses to first and fourth movement in A).

Figure 6. Simultaneous recordings of wrist extensor IEMG activity and wrist flexor tension responses during active repetitive wrist dorsiflexions

Dashed lines show tension base line (defined as in Fig. 5A) and resting wrist position (defined as in Fig. 1). Note the close correspondence between the strength of the short-range stiffness as exhibited by the flexor tension responses and the strength of the initial extensor activation required for movement generation.

Figure 2. Muscle activation patterns during active repetitive wrist dorsiflexions of similar triangular shape and amplitude as the passive movements shown in Fig. 1

A, dashed lines in wrist extensor IEMG trace drawn to highlight that the speed of the initial rise of EMG activity depends on whether the dorsiflexion movement is imposed after a period of rest or immediately after a preceding similar dorsiflexion movement. B, X-Y plot of extensor IEMG activity against wrist displacement for the three consecutive movements shown in A. The upper and the middle horizontal dashed line indicates the IEMG level at 2 deg of dorsiflexion for the first and the second movement, respectively. The two vertical dotted bars (to the right) indicate the IEMG amplitudes used for quantification.