Threshold position control of anticipation in humans: a possible role of corticospinal influences

Abstract

The role of corticospinal (CS) pathways in anticipatory motor actions was evaluated using transcranial magnetic stimulation (TMS) of the primary motor cortex projecting to motoneurons (MNs) of wrist muscles. Preloaded wrist flexors were suddenly unloaded by the experimenter or by the subject using the other hand (self-unloading). After sudden unloading, the wrist joint involuntarily flexed to a new position. In contrast, during self-unloading the wrist remained almost motionless, implying that an anticipatory postural adjustment occurred. In the self-unloading task, anticipation was manifested by a decrease in descending facilitation of pre-activated flexor MNs starting ∼72 ms before changes in the background EMG activity. Descending facilitation of extensor MNs began to increase ∼61 ms later. Conversely, these influences remained unchanged before sudden unloading, implying the absence of anticipation. We also tested TMS responses during EMG silent periods produced by brief muscle shortening, transiently resulting in similar EMG levels before the onset and after the end of self-unloading. We found reduced descending facilitation of flexor MNs after self-unloading. To explain why the wrist excursion was minimized in self-unloading due to these changes in descending influences, we relied on previous demonstrations that descending systems pre-set the threshold positions of body segments at which muscles begin to be activated, thus predetermining the equilibrium point to which the system is attracted. Based on this notion, a more consistent explanation of the kinematic, EMG and descending patterns in the two types of unloading is proposed compared to the alternative notion of direct pre-programming of kinematic and/or EMG patterns.

Vestibular and corticospinal control of human body orientation in the gravitational field

“…Whether these areas transmit changes in the referent body orientation may be a subject of future studies. Indeed, corticospinal influences in cooperation with other descending systems may be responsible for other changes in body posture and joint configurations not related to body orientation (e.g., Ilmane et al 2013;Raptis et al 2010;Sangani et al 2011;Zhang et al 2017b). For comparison, corticospinal reflexes were effective in maintaining the same vertical body orientation in quadrupeds (Beloozerova et al 2003;Deliagina et al 2006Deliagina et al , 2014, whereas intentional changes in this orientation could be produced in an open-loop way, without reflex-mediated changes in the state of the corticospinal system, as observed in our study.…”

Indirect, referent control of motor actions underlies directional tuning of neurons

“…The validity of different models and views can be evaluated not only on the basis of the above criteria but also by experimental testing. This has been done in several studies (Foisy and Feldman 2006;Ilmane et al 2013;Raptis et al 2010;Sangani et al 2011;Turpin et al 2016;Zhang et al 2017Zhang et al , 2018 with results inconsistent with the notion of preprogramming of the motor outcome, as illustrated in Fig. 6.…”

“…Intentional movements in humans also result from shifts in the spatial thresholds, i.e., the referent point of the FR (Asatryan and Feldman 1965). A series of recent experimental studies has specifically focused on changes in spatial thresholds in the control of posture and movement in humans (Foisy and Feldman 2006;Ilmane et al 2013;Mullick et al 2018;Raptis et al 2010;Sangani et al 2011;Turpin et al 2017;Zhang et al 2017Zhang et al , 2018.…”

“…The same principle underlies the solution of the posture-movement problem (see MOTONEURONS FUNCTION IN A SPATIAL FRAME OF REFERENCE). Strong support for the notion of parametric control of motor actions came from recent findings that corticospinal influences can be decorrelated from kinematic and kinetic variables, including EMG patterns, such that these influences only predetermine where, in the spatial domain or FR, ␣-MNs can be activated without any computation or predetermining of the motor outcome (Ilmane et al 2013;Raptis et al 2010;Sangani et al 2011;Turpin et al 2016;Zhang et al 2017Zhang et al , 2018.…”

“…This possibility follows from the empirically derived equilibrium-point hypothesis, now advanced to the theory of indirect, referent control of action and perception (Feldman 2015). Strong support to this theory as well as for indirect control of motor actions by M1 is derived from recent findings that corticospinal influences can be decorrelated from kinematic and kinetic variables, including EMG patterns, such that these influences only predetermine where, in the spatial domain or frame of reference (FR), ␣-MNs can be activated without predetermining the motor outcome (Ilmane et al 2013;Raptis et al 2010;Sangani et al 2011;Turpin et al 2016;Zhang et al 2017Zhang et al , 2018. Thus, although directional sensitivity of M1 neurons is an experimental fact, the assumption that these neurons directly predetermine the direction of hand movement or isometric force remains controversial.…”