The fusimotor and reafferent origin of the sense of force and weight

Abstract

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.

Sex-Specific Links in Motor and Sensory Adaptations to Repetitive Motion–Induced Fatigue

“…Studies of fatigue and/or sensory reweighting have proposed that altered afferent signaling contributes to the perception of effort (Luu, Day, Cole, & Fitzpatrick, 2011) and contributes to associated altered motor patterns (Carpenter, Murnaghan, & Inglis, 2010;Eva-Maj, Hans, Per-Anders, & Mikael, 2013). The results of our study are consistent in showing that disturbances of the sensory system, quantified by increases in sensory thresholds (i.e., declines in afferent signaling of event detection), are related to, and possibly part of, mechanisms influential in generating greater changes in motor patterns.…”

Role of Ratings of Perceived Exertion during Self-Paced Exercise: What are We Actually Measuring?

“…electromyography) during exercise is thought to be largely influenced by a central feed-forward neurophysiological mechanism whereby as motor unit recruitment and firing Reproduced from Swart et al [27], with permission frequency increase, the number of efferent copies received by sensory regions within the brain also increases [39,44,45]. This theory is supported by the relationship between perceptions of effort or exertion and the increase in central drive required to exercise at higher intensities and/or during periods of muscle weakening resulting from peripheral fatigue [46] or partial paralysis [47,48]. Indeed, we have recently shown that elevated peripheral fatigue and a concomitant increase in central drive is associated with an increase in RPE during constant-load, high-intensity cycling [46].…”

The senses of active and passive forces at the human ankle joint

“…It was postulated that if force sense arose entirely from a central mechanism (McCloskey 1981), accurate force matching should be achievable at such different lengths. On the other hand, if stretch receptor afferents contributed to force sense (Luu et al 2011), for the same level of motor command at the two lengths, the force perceived at the longer length should be greater. This would be a consequence of the increased afferent activity in the stretched muscle.…”

“…Alternatively, the sense of force may not be generated entirely centrally. It has recently been proposed that peripheral signals, including a component from muscle spindles, contribute to the sense of muscle force (Luu et al 2011). Here the authors saw the peripheral contribution, not as a pure exafference, rather as a reafference generated in response to the motor command.…”

“…The lengths have been so adjusted that active forces in the two legs match. The hypothesis is that if muscle stretch receptors contribute to the sense of force (Luu et al 2011;Brooks et al 2013), they should be more stretched at the longer muscle lengths and therefore generate more activity. It leads to the prediction that in a force matching task, the force generated in the leg with the longer muscle should be overestimated by the leg with the shorter muscle.…”