Convergence of proprioceptive and visual feedback on neurons in primary motor cortex

Cross, Kevin P.; Dj, Cook; Scott, SH

doi:10.1101/2021.05.01.442274

Cited by 15 publications

(17 citation statements)

References 111 publications

(160 reference statements)

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“…A large number of studies inspired by OFC highlight how humans are capable of generating fast, goal-directed motor corrections ( Cluff and Scott, 2015 ; Cross et al, 2019 ; Diedrichsen, 2007 ; Dimitriou et al, 2012 ; Kurtzer et al, 2008 ; Nashed et al, 2014 ; Scott, 2016 ) even for very small disturbances ( Crevecoeur et al, 2012 ) and OFC can capture features of unperturbed movements ( Knill et al, 2011 ; Lillicrap and Scott, 2013 ; Liu and Todorov, 2007 ; Nashed et al, 2012 ; Todorov and Jordan, 2002 ; Trommershäuser et al, 2005 ). Further studies highlight how feedback responses to a mechanical disturbance are distributed throughout somatosensory, parietal, frontal, and cerebellar motor circuits in ~20 ms and display goal-directed responses in as little as 60 ms ( Chapman et al, 1984 ; Conrad et al, 1975 ; Cross et al, 2021 ; Evarts and Tanji, 1976 ; Herter et al, 2009 ; Lemon, 1979 ; Omrani et al, 2016 ; Phillips et al, 1971 ; Pruszynski et al, 2011 ; Pruszynski et al, 2014 ; Strick, 1983 ; Wolpaw, 1980 ). Finally, a recent study demonstrates that inputs from motor thalamus to MC are essential for the execution of motor actions ( Sauerbrei et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Rotational dynamics in motor cortex are consistent with a feedback controller

Kalidindi

Cross

Lillicrap

et al. 2021

eLife

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Recent studies have identified rotational dynamics in motor cortex (MC), which many assume arise from intrinsic connections in MC. However, behavioral and neurophysiological studies suggest that MC behaves like a feedback controller where continuous sensory feedback and interactions with other brain areas contribute substantially to MC processing. We investigated these apparently conflicting theories by building recurrent neural networks that controlled a model arm and received sensory feedback from the limb. Networks were trained to counteract perturbations to the limb and to reach toward spatial targets. Network activities and sensory feedback signals to the network exhibited rotational structure even when the recurrent connections were removed. Furthermore, neural recordings in monkeys performing similar tasks also exhibited rotational structure not only in MC but also in somatosensory cortex. Our results argue that rotational structure may also reflect dynamics throughout the voluntary motor system involved in online control of motor actions.

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Section: Introductionmentioning

confidence: 99%

Rotational dynamics in motor cortex are consistent with a feedback controller

Kalidindi

Cross

Lillicrap

et al. 2021

eLife

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“…Thus, consistent with OFC visual feedback is processed initially by circuits involved with state estimation followed by circuits involved with implementing the control policy. However, there is evidence that visual feedback responses arrive first in premotor cortex (50-70ms) followed by M1 (70-100) and finally parietal area 5 (Cisek and Kalaska, 2005; Archambault et al, 2011; Ames et al, 2014; Stavisky et al, 2017; Cross et al, 2021). Thus, premotor cortex may generate the earliest muscle response to visual feedback rather than M1.…”

Section: Discussionmentioning

confidence: 99%

Proprioceptive and visual feedback responses in macaques exploit goal redundancy

Cross

Guang

Scott

2022

Preprint

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A common problem in motor control concerns how to generate patterns of muscle activity when there are redundant solutions to attain a behavioural goal. Optimal feedback control is a theory that has guided many behavioural studies exploring how the motor system incorporates task redundancy. This theory predicts that kinematic errors that deviate the limb should not be corrected if one can still attain the behavioural goal. Several studies in humans demonstrate that the motor system can flexibly integrate visual and proprioceptive feedback of the limb with goal redundancy within 90ms and 70ms, respectively. Here we show monkeys (Macaca mulatta) demonstrate similar abilities to exploit goal redundancy. We trained four male monkeys to reach for a goal that was either a narrow square or a wide, spatially redundant rectangle. Monkeys exhibited greater trial-by-trial variability when reaching to the wide goal consistent with exploiting goal redundancy. On random trials we jumped the visual feedback of the hand and found monkeys corrected for the jump when reaching to the narrow goal and largely ignored the jump when reaching for the wide goal. In a separate set of experiments, we applied mechanical loads to the arm and found similar corrective responses based on goal shape. Muscle activity reflecting these different corrective responses were detected for the visual and mechanical perturbations starting at ~90 and ~70ms, respectively. Thus, rapid motor responses in macaques can exploit goal redundancy similar to humans, creating a paradigm to study the neural basis of goal-directed motor action and motor redundancy.

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“…To perform the feedback control presented in Figure 1B, the candidate feedback controller must 1) receive sensory inputs 2) project to the muscles and 3) send an efference copy signal to the forward model. Motor cortical neurons receive substantial somatosensory input (Cross et al, 2021;Pavlides et al, 1993), and old-world primates (and humans) have direct projections from motor cortex to motor neurons (Lemon, 1997;Rathelot & Strick, 2009). The cortico-pontine mossy fibers provide the cerebellum with efference copy inputs (Ramnani, 2006).…”

Section: Motor Cortex As a Feedback Controllermentioning

confidence: 99%

“…The brain can adjust feedback gains according to planning and context, thereby altering the nature of the transformation of state estimates into motor output. Most research in this field has been at the level of movement psychophysics (Mazzoni & Krakauer, 2006;Sha et al, 2006;Taylor et al, 2014), only infrequently examining the firing rates of single neurons (Cross et al, 2021;Kalidindi et al, 2021;Pruszynski, 2014;Pruszynski et al, 2011). OFC presents what might be considered an "algorithm-level" description of how the motor system controls movements but is largely agnostic to how this algorithm is implemented by neurons.…”

Section: Introductionmentioning

confidence: 99%

Dynamical Feedback Control: Motor Cortex as an Optimal Feedback Controller Based on Neural Dynamics

Versteeg¹,

Miller²

2022

Preprint

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Primates have an unparalleled ability to produce a wide range of dexterous movements, each sensitive to context and robust to perturbation. Recent progress in understanding the neural basis of movement generation comes from two largely independent ideas, “Optimal Feedback Control” and “Neural Dynamical Systems”. The optimal control framework was largely inspired by research programs from the ‘80s showing that the brain doesn’t seem to plan a simple desired movement trajectory, but instead produces movements by transforming sensory information into motor output that satisfies an optimality criterion. The more recent idea that the motor cortex acts as a dynamical system came about only as it became possible to analyze large numbers of simultaneously recorded single neurons. These two framings of the motor system have been largely incommensurate, neither able to contribute much to the understanding of the other. In this review, we reconcile these two views into a single model we call “Dynamical Feedback Control”. We propose that the dynamics in the motor cortex emerge from a sensorimotor transformation that couples the motor cortex to sensory input from the periphery, and to contextual inputs from other cortical and subcortical areas. Dynamics in motor cortex can be thought to approximate gains of a feedback controller, and by moving the neural state to different regions of state space, the motor system can rapidly alternate between different controllers. The DFC framework presents a new lens to interpret neural dynamics, and to understand how ensembles of neurons generate flexible and responsive patterns of muscle activity.

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Convergence of proprioceptive and visual feedback on neurons in primary motor cortex

Cited by 15 publications

References 111 publications

Rotational dynamics in motor cortex are consistent with a feedback controller

Rotational dynamics in motor cortex are consistent with a feedback controller

Proprioceptive and visual feedback responses in macaques exploit goal redundancy

Dynamical Feedback Control: Motor Cortex as an Optimal Feedback Controller Based on Neural Dynamics

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