Re-thinking the role of motor cortex: context-sensitive motor outputs?
The standard account of motor control considers descending outputs from primary motor cortex (M1) as motor commands and efference copy. This account has been challenged recently by an alternative formulation in terms of active inference: M1 is considered as part of a sensorimotor hierarchy providing top-down proprioceptive predictions. The key difference between these accounts is that predictions are sensitive to the current proprioceptive context, whereas efference copy is not. Using functional electric stimulation to experimentally manipulate proprioception during voluntary movement in healthy human subjects, we assessed the evidence for context sensitive output from M1. Dynamic causal modeling of functional magnetic resonance imaging responses showed that FES altered proprioception increased the influence of M1 on primary somatosensory cortex (S1). These results disambiguate competing accounts of motor control, provide some insight into the synaptic mechanisms of sensory attenuation and may speak to potential mechanisms of action of FES in promoting motor learning in neurorehabilitation.
Politecnico di Milano, NearLab, Department of Electronics, Information and Bioengineering, Via G. Colombo 40, 20133 Milano, Italy. Electronic address: marta.gandolla@polimi.it.
Marta
M
Gandolla
Politecnico di Milano, NearLab, Department of Electronics, Information and Bioengineering, Via G. Colombo 40, 20133 Milano, Italy. Electronic address: simona.ferrante@polimi.it.
Simona
S
Ferrante
Valduce Hospital, Villa Beretta Rehabilitation Center, Via N. Sauro 17, 23845 Costamasnaga, LC, Italy. Electronic address: fmolteni@valduce.it.
Franco
F
Molteni
Valduce Hospital, Villa Beretta Rehabilitation Center, Via N. Sauro 17, 23845 Costamasnaga, LC, Italy. Electronic address: eleonora.guanziroli@gpop.it.
Eleonora
E
Guanziroli
Valduce Hospital, Unità Operativa Complessa di Radiologia, via D. Alighieri 11, 22100 Como, Italy. Electronic address: tfrattini@valduce.it.
Tiziano
T
Frattini
Valduce Hospital, Unità Operativa Complessa di Radiologia, via D. Alighieri 11, 22100 Como, Italy. Electronic address: amartegani@valduce.it.
Alberto
A
Martegani
Politecnico di Milano, NearLab, Department of Electronics, Information and Bioengineering, Via G. Colombo 40, 20133 Milano, Italy. Electronic address: giancarlo.ferrigno@polimi.it.
Giancarlo
G
Ferrigno
Wellcome Trust Centre for Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK. Electronic address: k.friston@ucl.ac.uk.
Karl
K
Friston
Politecnico di Milano, NearLab, Department of Electronics, Information and Bioengineering, Via G. Colombo 40, 20133 Milano, Italy. Electronic address: alessandra.pedrocchi@polimi.it.
Alessandra
A
Pedrocchi
Sobell Department of Movement Neuroscience, UCL Institute of Neurology, 33 Queen Square, London WC1N 3BG, UK. Electronic address: n.ward@ucl.ac.uk.
Nick S
NS
Ward
D000328:Adult; D001696:Biomechanical Phenomena; D004525:Efferent Pathways / Q000502:physiology*; D004558:Electric Stimulation; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D007858:Learning; D007866:Leg / Q000294:innervation; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D008959:Models, Neurological; D009044:Motor Cortex / Q000502:physiology*; D011187:Posture / Q000502:physiology; D011434:Proprioception / Q000502:physiology; D013003:Somatosensory Cortex / Q000502:physiology; D013569:Synapses / Q000502:physiology; D055815:Young Adult
Functional electrical stimulation; Motor cortex; Proprioception