A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world1–4. This local-to-global problem is also fundamental to motor control of the arm since complex mechanical interactions between the shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques5 (Fig. 1a). Here we show 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 which appropriately counter the underlying torque within ~50 ms 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 ms after pure elbow displacement can be potentiated by transcranial magnetic stimulation. Our results show that M1 underlies multi-joint integration during fast feedback control, demonstrating that transcortical processing permits feedback responses to express a level of sophistication previously reserved for voluntary control and providing neurophysiological support for influential theories positing that voluntary movement is generated by the intelligent manipulation of sensory feedback6,7.
Many human studies have demonstrated that rapid motor responses (i.e., muscle-stretch reflexes) to mechanical perturbations can be modified by a participant's intended response. Here, we used a novel experimental paradigm to investigate the neural mechanisms that underlie such goal-dependent modulation. Two monkeys positioned their hand in a central area against a constant load and responded to mechanical perturbations by quickly placing their hand into visually defined spatial targets. The perturbation was chosen to excite a particular proximal arm muscle or isolated neuron in primary motor cortex and two targets were placed so that the hand was pushed away from one target (OUT target) and toward the other (IN target). We chose these targets because they produced behavioral responses analogous to the classical verbal instructions used in human studies. A third centrally located target was used to examine responses with a constant goal. Arm muscles and neurons robustly responded to the perturbation and showed clear goal-dependent responses ϳ35 and 70 ms after perturbation onset, respectively. Most M1 neurons and all muscles displayed larger perturbation-related responses for the OUT target than the IN target. However, a substantial number of M1 neurons showed more complex patterns of target-dependent modulation not seen in muscles, including greater activity for the IN target than the OUT target, and changes in target preference over time. Together, our results reveal complex goal-dependent modulation of fast feedback responses in M1 that are present early enough to account for goal-dependent stretch responses in arm muscles.
Corrective responses to limb disturbances are surprisingly complex, but the neural basis of these goal-directed responses is poorly understood. Here we show that somatosensory feedback is transmitted to many sensory and motor cortical regions within 25 ms of a mechanical disturbance applied to the monkey's arm. When limb feedback was salient to an ongoing motor action (task engagement), neurons in parietal area 5 immediately (~25 ms) increased their response to limb disturbances, whereas neurons in other regions did not alter their response until 15 to 40 ms later. In contrast, initiation of a motor action elicited by a limb disturbance (target selection) altered neural responses in primary motor cortex~65 ms after the limb disturbance, and then in dorsal premotor cortex, with no effect in parietal regions until 150 ms post-perturbation. Our findings highlight broad parietofrontal circuits that provide the neural substrate for goal-directed corrections, an essential aspect of highly skilled motor behaviors.
Primary motor cortex has been studied for more than a century, yet a consensus on its functional contribution to movement control is still out of reach. In particular, there remains controversy as to the level of control produced by motor cortex ("low-level" movement dynamics vs. "high-level" movement kinematics) and the role of sensory feedback. In this review, we present different perspectives on the two following questions: What does activity in motor cortex reflect? and How do planned motor commands interact with incoming sensory feedback during movement? The four authors each present their independent views on how they think the primary motor cortex (M1) controls movement. At the end, we present a dialogue in which the authors synthesize their views and suggest possibilities for moving the field forward. While there is not yet a consensus on the role of M1 or sensory feedback in the control of upper limb movements, such dialogues are essential to take us closer to one.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.