To Move or Not to Move? Functional Role of Ventral Premotor Cortex in Motor Monitoring During Limb Immobilization

Abstract

Anatomo-clinical evidence from motor-awareness disorders after brain-damages suggests that the premotor cortex (PMC) is involved in motor-monitoring of voluntary actions. Indeed, PMC lesions prevent patients from detecting the mismatch between intended, but not executed, movements with the paralyzed limb. This functional magnetic resonance imaging study compared, in healthy subjects, free movements against blocked movements, precluded by a cast. Cast-related corticospinal excitability changes were investigated by using transcranial magnetic stimulation. Immediately after the immobilization, when the cast prevented the execution of left-hand movements, the contralateral right (ventral) vPMC showed both increased hemodynamic activity and increased functional connectivity with the hand area in the right somatosensory cortex, suggesting a vPMC involvement in detecting the mismatch between planned and executed movements. Crucially, after 1 week of immobilization, when the motor system had likely learned that no movement could be executed and, therefore, predictions about motor consequences were changed, vPMC did not show the enhanced activity as if no incongruence has to be detected. This can be interpreted as a consequence of the plastic changes induced by long-lasting immobilization, as also proved by the cast-related corticospinal excitability modulation in our subjects. The present findings highlight the crucial role of vPMC in the anatomo-functional network generating the human motor-awareness.

Direct electrical stimulation of the premotor cortex shuts down awareness of voluntary actions

“…4a). This structural temporofronto-parietal connectivity pattern is highly compatible with the role of ventral PMC as a comparator system 2,7-9 , proposed by lesion studies in AHP patients 2,7-9 and by neuroimaging studies in healthy subjects 32,[44][45][46][47] . For instance, ventral PMC has been recently described as the neural correlate of motor-monitoring during mechanical limb immobilization.…”

“…(1) A positive effect in altering motor execution was expected based on previous literature employing DES during the same HMt 12,14,15 . (2) A positive effect in altering the motor awareness was expected based on anatomical and functional evidence in AHP patients 2,7-9,48,49 and in healthy subjects 44,45 . It is important to note that lesion studies in AHP patients also highlight the role of other brain areas putatively relevant for motor unawareness, such as the temporo-parietal junction 48 and the insula 48,50 .…”

“…For instance, ventral PMC has been recently described as the neural correlate of motor-monitoring during mechanical limb immobilization. The increased ventral PMC activity during impossible movements has been related to conscious detection of the mismatch between movement planning and (no) movement execution 44 . According to this comparator model the hypothesis is that once the motor command is ready to be issued, an efference copy of the movement is generated in motor planning areas (e.g., SMA and dorsal PMC) and, on the basis of this signal, a forward model predicts the sensory consequences of the action.…”

“…When the movement is implemented, the afferent inputs coming from muscle contractions reach S1, which, in turn, send sensory feedback to PPC, where sensory information converges. Finally, the sensory information of the movement is sent, through fronto-parietal connections, from the PPC, to the ventral PMC, which should compare the actual sensory input with the sensory predictions generated by the forward model 32,44 . This comparison may eventually lead to a veridical motor awareness (in our context, it leads the patient to recognize, as during S1 stimulation, that no movement has been performed and to say STOP).…”

Losing my hand. Body ownership attenuation after virtual lesion of the primary motor cortex

“…Interestingly, in that study, it has been also found an enhanced/more rigid sense of body ownership for the (healthy) not immobilized hand (where the strength of the RHI is decreased). According to previous TMS studies on both immobilization procedure in healthy subjects (Avanzino, Bassolino, Pozzo, & Bove, ) and constraint‐induced movement therapy (CIMT) in brain‐damaged patients (Wittenberg & Schaechter, ), which showed increased activity of the hemisphere ipsilateral to the immobilized limb (for a different result see Garbarini et al., ), the decreased RHI susceptibly for the intact hand of hemiplegic patients can be due to hyper‐use of the intact side. If this is the case, future experiments assessing the complementary effect of high‐frequency rTMS, known to increase the M1 corticospinal excitability (Arai et al., ; Maeda, Keenan, Tormos, Topka, & Pascual‐Leone, ), should document a reduced RHI susceptibility.…”