Signals associated with the command the brain sends to muscles are thought to create the sensation of heaviness when we lift an object. Thus, as a muscle is weakened by fatigue or partial paralysis (neuromuscular blockade), the increase in the motor command needed to lift a weight is thought to explain the increasing subjective heaviness of the lifted object.With different fatiguing contractions we approximately halved the force output of the thumb flexor muscles, which were then used to lift an object. For two deafferented subjects the perceived heaviness of the lifted object approximately doubled, in keeping with the central-signal theory. However, for normal subjects this resulted in objects feeling the same or lighter, inconsistent with the central-signal theory but consistent with the expected effects of the conditioning contractions on the sensitivity of peripheral receptors. In separate experiments we subjected the forearm muscles to complete paralysis with a non-depolarising neuromuscular blocking agent and then allowed them to recover to approximately half-force output. This also resulted in objects feeling lighter when lifted by the semi-paralysed thumb, even though the motor command to the motoneurons must have been greater. This is readily explained by reduced lift-related reafference caused by the prolonged paralysis of muscle spindle intrafusal fibres.We conclude that peripheral signals, including a major contribution from muscle spindles, normally give rise to the sense of exerted force. In concept, however, reafference from peripheral receptors may also be considered a centrally generated signal that traverses efferent and then afferent pathways to feed perceptual centres rather than one confined entirely to the central nervous system. These results therefore challenge the distinction between central- and peripheral-based perception, and the concept that muscle spindles provide only information about limb position and movement.
Dakin CJ, Luu BL, van den Doel K, Inglis JT, Blouin J-S. Frequency-specific modulation of vestibular-evoked sway responses in humans. J Neurophysiol 103: 1048 -1056, 2010. First published December 23, 2009 doi:10.1152/jn.00881.2009. Galvanic vestibular stimulation (GVS) results in characteristic muscle and whole-body responses in humans maintaining standing balance. However, the relationship between these two vestibular-evoked responses remains elusive. This study seeks to determine whether mechanical filtering from conversion of lower-limb muscle activity to body sway, during standing balance, can be used to attenuate sway while maintaining biphasic lower-limb muscle responses using frequency-limited stochastic vestibular stimulation (SVS). We hypothesized that SVS deprived of frequencies Ͻ2 Hz would evoke biphasic muscle responses with minimal whole-body sway due to mechanical filtering of the higher-frequency muscle responses. Subjects were exposed to five stimulus bandwidths: two meant to induce sway responses (0 -1 and 0 -2 Hz) and three to dissociate vestibular-evoked muscle responses from whole-body sway (0 -25, 1-25, and 2-25 Hz). Two main results emerged: 1) SVS-related sway was attenuated when frequencies Ͻ2 Hz were excluded, whereas multiphasic muscle and force responses were retained; and 2) the gain of the estimated transfer functions exhibited successive low-pass filtering of vestibular stimuli during conversion to muscle activity, anteroposterior (AP) moment, and sway. This successive low-pass filtering limited the transfer of signal power to frequencies Ͻ20 Hz in muscle activity, Ͻ5 Hz in AP moment, and Ͻ2 Hz in AP trunk sway. Consequently, the present results show that SVS delivered at frequencies Ͼ2 Hz to standing humans do not cause a destabilizing whole-body sway response but are associated with the typical biphasic lower-limb muscle responses.
During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscle's ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances.
Key points• Electrical vestibular stimulation delivered at the mastoid processes evokes a reflex response in the appendicular muscles only when they are actively involved in keeping the unsupported head and body balanced.• We show that the vestibular-evoked muscle response was present during a task that simulated the control of standing where sensory feedback was congruent with the motor-generated expectation to balance the body, and absent when sensory feedback did not match.• The present results indicate that the task dependency of the vestibular-evoked muscle response relies on congruent sensory and motor signals, and that this is organised in the absence of a conscious perception of postural control.• These findings help us understand how our brain combines sensory and motor signals to provide an internal representation of standing balance that can be used to assess whether a perturbation poses a postural threat.Abstract We investigate whether the muscle response evoked by an electrically induced vestibular perturbation during standing is related to congruent sensory and motor signals. A robotic platform that simulated the mechanics of a standing person was used to manipulate the relationship between the action of the calf muscles and the movement of the body. Subjects braced on top of the platform with the ankles sway referenced to its motion were required to balance its simulated body-like load by modulating ankle plantar-flexor torque. Here, afferent signals of body motion were congruent with the motor command to the calf muscles to balance the body. Stochastic vestibular stimulation (±4 mA, 0-25 Hz) applied during this task evoked a biphasic response in both soleus muscles that was similar to the response observed during standing for all subjects. When the body was rotated through the same motion experienced during the balancing task, a small muscle response was observed in only the right soleus and in only half of the subjects. However, the timing and shape of this response did not resemble the vestibular-evoked response obtained during standing. When the balancing task was interspersed with periods of computer-controlled platform rotations that emulated the balancing motion so that subjects thought that they were constantly balancing the platform, coherence between the input vestibular stimulus and soleus electromyogram activity decreased significantly (P < 0.05) during the period when plantar-flexor activity did not affect the motion of the body. in coherence occurred at 175 ms after the transition to computer-controlled motion, which subjects did not detect until after 2247 ms (Confidence Interval 1801, 2693), and then only half of the time. Our results indicate that the response to an electrically induced vestibular perturbation is organised in the absence of conscious perception when sensory feedback is congruent with the underlying motor behaviour.
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