Shared internal models for feedforward and feedback control of arm dynamics in non‐human primates

Abstract

Previous work has shown that humans account for and learn novel properties or the arm's dynamics, and that such learning causes changes in both the predictive (i.e., feedforward) control of reaching and reflex (i.e., feedback) responses to mechanical perturbations. Here we show that similar observations hold in old‐world monkeys (Macaca fascicularis). Two monkeys were trained to use an exoskeleton to perform a single‐joint elbow reaching and to respond to mechanical perturbations that created pure elbow motion. Both of these tasks engaged robust shoulder muscle activity as required to account for the torques that typically arise at the shoulder when the forearm rotates around the elbow joint (i.e., intersegmental dynamics). We altered these intersegmental arm dynamics by having the monkeys generate the same elbow movements with the shoulder joint either free to rotate, as normal, or fixed by the robotic manipulandum, which eliminates the shoulder torques caused by forearm rotation. After fixing the shoulder joint, we found a systematic reduction in shoulder muscle activity. In addition, after releasing the shoulder joint again, we found evidence of kinematic aftereffects (i.e., reach errors) in the direction predicted if failing to compensate for normal arm dynamics. We also tested whether such learning transfers to feedback responses evoked by mechanical perturbations and found a reduction in shoulder feedback responses, as appropriate for these altered arm intersegmental dynamics. Demonstrating this learning and transfer in non‐human primates will allow the investigation of the neural mechanisms involved in feedforward and feedback control of the arm's dynamics.

Contextual cues are not unique for motor learning: Task-dependant switching of feedback controllers

“…As multiple recent papers have demonstrated that voluntary (feedforward) and feedback control likely share neural circuits [ 24 , 39 , 64 – 67 ], it is reasonable to believe that similar contextual regulation would also be present in feedback control. However, studies that have shown this parallel changes in the feedback responses to the learning of the feedforward dynamics, either examined before and after adaptation to novel dynamics [ 24 , 64 , 68 , 69 ], or during the process of adaptation [ 19 , 70 – 72 ], meaning that the they could not distinguish between the slow adaptation of the feedback controller to each condition or the rapid switching between two controllers. Moreover, other studies have suggested that feedforward and feedback controllers are learned separately [ 73 , 74 ] and may even compete with one another [ 75 ], suggesting that these share different neural circuits and may have different properties.…”

Proprioceptive and visual feedback responses in macaques exploit goal redundancy

“…Muscle activity evoked by the mechanical loads exhibit similar patterns as the control output with an initial increase starting at ~50ms followed by differentiation based on goal shape starting at ~70ms in both humans (Nashed et al, 2012) and monkeys (present study). Other studies have also found humans and monkeys exhibit similar timing for when corrective responses to mechanical loads are modulated by different contexts including for limb physics (Kurtzer et al, 2008;Pruszynski et al, 2011), task instruction (Hammond, 1956;Evarts and Tanji, 1976;Pruszynski et al, 2008Pruszynski et al, , 2014Omrani et al, 2014), and adaptation (Cluff and Scott, 2013;Maeda et al, 2018Maeda et al, , 2020) which all start 60-70ms after the onset of the load. This similarity highlights how monkeys are a useful model to investigate the neural circuits that underlie flexible feedback processing during motor actions.…”

Myomatrix arrays for high-definition muscle recording

“…On 10% of trials no perturbation was applied, and the monkey had to maintain the hand in the central target. In addition to Myomatrix injectables, we acquired bipolar electromyographic activity from nonhuman primates using intramuscular fine-wire electrodes in the biceps brachii long head as described previously (Maeda, Kersten, and Pruszynski 2021), recording in this instance from the same biceps muscle in the same animal from which we also collected Myomatrix data, although in a separate recording session. Electrodes were spaced ~8 mm apart and aligned to the muscle fibers, and a reference electrode was inserted subcutaneously in the animal's back.…”