Primary motor cortex underlies multi-joint integration for fast feedback control

• Published in: Nature (London) Vol. 478; no. 7369; pp. 387 - 390
• Main Authors: Pruszynski, J. Andrew, Kurtzer, Isaac, Nashed, Joseph Y., Omrani, Mohsen, Brouwer, Brenda, Scott, Stephen H.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.09.2011; Nature Publishing Group
• Subjects: 631/378/1697; 631/378/2629; 631/378/2632/1663; Adult; Animals; Biological and medical sciences; Biomechanical Phenomena - physiology; Elbow - physiology; Electrodes; Evoked Potentials, Motor - physiology; Experiments; Feedback, Sensory - physiology; Female; Fundamental and applied biological sciences. Psychology; Human subjects; Humanities and Social Sciences; Humans; letter; Macaca mulatta; Male; Mechanical properties; Motor control and motor pathways. Reflexes. Control centers of vegetative functions. Vestibular system and equilibration; Motor Cortex - cytology; Motor Cortex - physiology; Motor Neurons - physiology; multidisciplinary; Muscle, Skeletal - physiology; Neurons; Science; Science (multidisciplinary); Shoulder; Shoulder - physiology; Time Factors; Vertebrates: nervous system and sense organs; Human; Integration; Transcranial magnetic stimulation; Central nervous system; Monkey; Feedback regulation; Nervous system; Cognition; Joint; Motor control; Encephalon; Osteoarticular system; Vertebrata; Mammalia; Feedback; Motor cortex; Shoulder; Primates; Perception; Motricity; Ambiguity
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/nature10436

Joint movement tracked by a feedback pathway For animals with multi-joint limbs, one of the daunting problems that the nervous system has to solve is how to correctly interpret and respond to sensory input induced by complex combinations of limb movements. For example, one apparently simple displacement of the shoulder could arise from an infinite number of different combinations of forces acting at the shoulder and elbow. Pruszynski et al . use neurophysiological recordings in monkeys and stimulation studies in humans to demonstrate that knowledge of limb mechanics is solved through a feedback pathway involving the primary motor cortex (M1), rather than through the feed-forward processing of motion variables, a view which has been dominant for the past 25 years. The results have implications for the design of humanoid robots and brain–machine interfaces, as well as for understanding and treating patients with motor dysfunctions such as stroke. A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world 1 , 2 , 3 , 4 . This local-to-global problem is also fundamental to motor control of the arm, because complex mechanical interactions between shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques 5 . Here we show, in humans and rhesus monkeys, that a transcortical pathway through primary motor cortex (M1) resolves this ambiguity during fast feedback control. We demonstrate that single M1 neurons of behaving monkeys can integrate shoulder and elbow motion information into motor commands that appropriately counter the underlying torque within about 50 milliseconds of a mechanical perturbation. Moreover, we reveal a causal link between M1 processing and multi-joint integration in humans by showing that shoulder muscle responses occurring ∼50 milliseconds after pure elbow displacement can be potentiated by transcranial magnetic stimulation. Taken together, our results show that transcortical processing through M1 permits feedback responses to express a level of sophistication that rivals voluntary control; this provides neurophysiological support for influential theories positing that voluntary movement is generated by the intelligent manipulation of sensory feedback 6 , 7 .