Single reach plans in dorsal premotor cortex during a two-target task

Dekleva, Brian M; Kording, Konrad; Miller, Lee E.

doi:10.1038/s41467-018-05959-y

Cited by 75 publications

(90 citation statements)

References 62 publications

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“…Subspaces enable inputs to co-exist with ongoing population activity. Although inputs, whether sensory 5,29 or cognitive such as during changes of mind 30,31 , influence motor cortical activity, the mechanisms that allow these inputs to coexist with ongoing population activity driving behavior have remained unclear. Intriguingly, motor cortex is dominated by apparently feedforward dynamics during the execution of planned or repetitive movements 14,17,18 .…”

Section: Discussionmentioning

confidence: 99%

Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

Conti

Badi

Bogaard

et al. 2020

Preprint

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Behavior relies on continuous influx of sensory information about the body and the environment. In primates, cortex integrates somatic feedback to accurately reach and manipulate objects. Yet, in many experimental regimes motor cortex seems paradoxically to operate as a feedforward, rather than feedback-driven, system. Here, we recorded simultaneously from motor and somatosensory cortex as monkeys performed a naturalistic reaching and object interaction behavior. We studied how unexpected feedback from behavioral errors influences cortical dynamics. Motor cortex generally exhibited robust feedforward dynamics, yet displayed feedback-driven dynamics surrounding correction of behavioral errors. We then decomposed motor cortical activity into orthogonal subspaces capturing communication with somatosensory cortex or behavior-generating dynamics. During error correction, the communication subspace became feedback-driven, while the behavioral subspace maintained feedforward dynamics. We therefore demonstrate that cortical activity is compartmentalized within distinct subspaces that shape the population dynamics, enabling flexible integration of salient inputs with ongoing activity for robust behavior.

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Section: Discussionmentioning

confidence: 99%

Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

Conti

Badi

Bogaard

et al. 2020

Preprint

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“…According to the influential affordance competition hypothesis (Cisek, 2012(Cisek, , 2007Cisek and Kalaska, 2010;Thura and Cisek, 2014), the brain specifies motor goals for competing options, in parallel, before deciding which one to execute (see also Klaes et al, 2011;Suriya-Arunroj and Gail, 2019). Although a number of behavioural and neurophysiological studies have expressed support for this hypothesis, alternative interpretations of the results of this work have been put forward; arguing that only a single motor goal is specified prior to target selection (Dekleva et al, 2018) or that the motor goal is specified only after target selection (Gallivan et al, 2018). Support for the affordance competition hypothesis comes from single cell recording studies that have employed delayed reach tasks in which one of two potential targets is cued after a preview period.…”

Section: Introductionmentioning

confidence: 92%

“…Importantly, most individual participants exhibited a mixture of encoding strategies across trials. This variability both within and across participants challenges that notion that any single model-i.e., parallel specification (e.g., Cisek, 2012), stay-or-switch (Dekleva et al, 2018) or serial-can account for participant behaviour.…”

Section: Target and Aimpoint Fixation Probabilitiesmentioning

confidence: 99%

“…These studies have found that, prior to target selection, competing potential reach targets appear to be represented in parallel in brain areas thought to be directly involved in movement execution, including dorsal premotor cortex (Cisek and Kalaska, 2005;Coallier et al, 2015;Pastor-Bernier and Cisek, 2011) and the parietal reach region (Klaes et al, 2011). However, this parallel specification interpretation has recently been challenged by a study that simultaneously recorded activity from populations of neurons in dorsal premotor cortex during a delayed reach task with two potential targets (Dekleva et al, 2018). The authors of this study argued that the apparent parallel representation of competing targets is an artifact of averaging across trials, and that, at the level of single trials, neural population activity is more consistent with only a single potential target being represented.…”

Section: Introductionmentioning

confidence: 99%

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Gaze Behaviour Reveals Flexible Encoding of Competing Reach Goals Under Conditions of Target Uncertainty

Brouwer

Smail

et al. 2020

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In daily tasks, we are often confronted with competing potential targets and must select one to act on. It has been suggested that, prior to target selection, the human brain encodes the motor goals of multiple, potential targets. However, this view remains controversial and it has been argued that only a single motor goal is encoded, or that motor goals are only specified after target selection. To investigate this issue, we measured participants’ gaze behaviour while viewing two potential reach targets, one of which was cued after a preview period. We applied visuomotor rotations to dissociate each visual target location from its corresponding motor goal location; i.e., the location participants needed to aim their hand toward to bring the rotated cursor to the target. During the preview period, participants most often fixated both motor goals but also frequently fixated one, or neither, motor goal location. Further gaze analysis revealed that on trials in which both motor goals were fixated, both locations were held in memory simultaneously. These findings show that, at the level of single trials, the brain most often encodes multiple motor goals prior to target selection, but may also encode either one or no motor goals. This result may help reconcile a key debate concerning the specification of motor goals in cases of target uncertainty.

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“…However, these averaged reach movements can 79 be abolished by changes to either task instructions or constraints (Hudson et al, 2007;Chapman 80 and Goodale, 2010), suggesting that the averaged movement may reflect an optimal task strategy 81 rather than a competition between two motor plans (Wong and Haith, 2017). More 82 fundamentally, the neurophysiological evidence for multiple potential reach plans has recently 83 been questioned (Dekleva et al, 2018) in that the observed averaging may be an artifact caused 84 by combining neural activity across multiple trials rather than examining activity on an 85 individual trial-by-trial basis. Thus, it is still debated whether similar rules apply for saccades 86 and reaches when the brain has to resolve multiple potential motor plans.…”

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confidence: 99%

Single-trial dynamics of competing reach plans in the human motor periphery

Medendorp

2019

Preprint

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Contemporary theories of motor control have suggested that multiple motor commands compete for action selection. While most of these competitions are completed prior to movement onset, averaged saccadic eye movements that land at an intermediate location between two visual targets are thought to arise when a movement is initiated prior to the resolution of the competition. In contrast, while averaged reach movements have been reported, there is still debate on whether averaged reach movements are the result of a resolved competition between two potential actions or a strategic behavior that optimally incorporates the current task demands. Here, we use a reach version of the paradigm that has previously shown to elicit saccadic averaging to examine whether similar averaging occurs based on neuromuscular activity of an upper limb muscle. On a single trial basis, we observed a temporal evolution of the two competing motor commands during a free-choice reach task to one of two visual targets. The initial wave of directionally-tuned muscle activity (∼100 ms after target onset) was an averaged of the two motor commands which then transformed into a single goal-directed motor command at the onset of the voluntary reach (∼200-300 ms after target onset). The transition from an early motor command to a single goal-direct command resembled the fact that saccadic averaging was most prominent for short-latency saccades. Further, the idiosyncratic choice made on a given trial was correlated with the biases in the averaged motor command.

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Single reach plans in dorsal premotor cortex during a two-target task

Cited by 75 publications

References 62 publications

Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

Motor cortical dynamics are shaped by multiple distinct subspaces during naturalistic behavior

Gaze Behaviour Reveals Flexible Encoding of Competing Reach Goals Under Conditions of Target Uncertainty

Single-trial dynamics of competing reach plans in the human motor periphery

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