Structure in Neural Activity during Observed and Executed Movements Is Shared at the Neural Population Level, Not in Single Neurons

Jiang, Xiyuan; Saggar, Hemant; Ryu, Stephen I.; Shenoy, Krishna V.; Kao, Jennifer L.

doi:10.1016/j.celrep.2020.108006

Cited by 39 publications

(33 citation statements)

References 73 publications

(144 reference statements)

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“…Typically, a mirror neuron fires both when individual acts and when the individual observes the same action performed by another. That is, the mirror neuron is believed to mediate the understanding of others’ behavior ( Jerjian et al, 2020 ; Jiang et al, 2020 ; Pezzulo et al, 2022 ). By contrast, the role of causal inference neurons in our study was putatively participating in self-identification and self-other discrimination.…”

Section: Discussionmentioning

confidence: 99%

Neural dynamics of causal inference in the macaque frontoparietal circuit

Fang

et al. 2022

eLife

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Natural perception relies inherently on inferring causal structure in the environment. However, the neural mechanisms and functional circuits essential for representing and updating the hidden causal structure and corresponding sensory representations during multisensory processing are unknown. To address this, monkeys were trained to infer the probability of a potential common source from visual and proprioceptive signals based on their spatial disparity in a virtual reality system. The proprioceptive drift reported by monkeys demonstrated that they combined previous experience and current multisensory signals to estimate the hidden common source and subsequently updated the causal structure and sensory representation. Single-unit recordings in premotor and parietal cortices revealed that neural activity in the premotor cortex represents the core computation of causal inference, characterizing the estimation and update of the likelihood of integrating multiple sensory inputs at a trial-by-trial level. In response to signals from the premotor cortex, neural activity in the parietal cortex also represents the causal structure and further dynamically updates the sensory representation to maintain consistency with the causal inference structure. Thus, our results indicate how the premotor cortex integrates previous experience and sensory inputs to infer hidden variables and selectively updates sensory representations in the parietal cortex to support behavior. This dynamic loop of frontal-parietal interactions in the causal inference framework may provide the neural mechanism to answer long-standing questions regarding how neural circuits represent hidden structures for body awareness and agency.

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Section: Discussionmentioning

confidence: 99%

Neural dynamics of causal inference in the macaque frontoparietal circuit

Fang

et al. 2022

eLife

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“…These findings emphasized the similarity between the neural codes for observed and executed actions, that is, the visual and motor formats. Nonetheless, subsequent studies have shown that MNs in various nodes of the action observation network (AON) (2) can exhibit visual responses to actions performed with tools (3,4), actions implied by moving cues (5)(6)(7)(8)(9)(10), or even withheld actions signaled by an instructive cue (11,12), suggesting a greater flexibility and broader relationship between the visual and motor codes.…”

Section: Introductionmentioning

confidence: 99%

Largely shared neural codes for biological and nonbiological observed movements but not for executed actions in monkey premotor areas

Albertini

Lanzilotto

Maranesi

et al. 2021

Journal of Neurophysiology

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The neural processing of others' observed actions recruits a large network of brain regions (the action observation network, AON), in which frontal motor areas are thought to play a crucial role. Since the discovery of mirror neurons (MNs) in the ventral premotor cortex, it has been assumed that their activation was conditional upon the presentation of biological rather than nonbiological motion stimuli, supporting a form of direct visuomotor matching. Nonetheless, nonbiological observed movements have rarely been used as control stimuli to evaluate visual specificity, thereby leaving the issue of similarity among neural codes for executed actions and biological or nonbiological observed movements unresolved. Here, we addressed this issue by recording from two nodes of the AON that are attracting increasing interest, namely the ventro-rostral part of the dorsal premotor area F2 and the mesial pre-supplementary motor area F6 of macaques while they 1) executed a reaching-grasping task, 2) observed an experimenter performing the task, and 3) observed a nonbiological effector moving in the same context. Our findings revealed stronger neuronal responses to the observation of biological than nonbiological movement, but biological and nonbiological visual stimuli produced highly similar neural dynamics and relied on largely shared neural codes, which in turn remarkably differed from those associated with executed actions. These results indicate that, in highly familiar contexts, visuo-motor remapping processes in premotor areas hosting MNs are more complex and flexible than predicted by a direct visuomotor matching hypothesis.

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“…Recent work suggests that the shape of the manifold on which neural states lie can reveal important features of the underlying dynamics of the system [ 70 – 72 , 137 – 142 ]. We believe the same holds for our data, particularly regarding the difference between the shapes of the decision manifolds in PMd versus M1.…”

Section: Discussionmentioning

confidence: 99%

Integrated neural dynamics of sensorimotor decisions and actions

et al. 2022

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Recent theoretical models suggest that deciding about actions and executing them are not implemented by completely distinct neural mechanisms but are instead two modes of an integrated dynamical system. Here, we investigate this proposal by examining how neural activity unfolds during a dynamic decision-making task within the high-dimensional space defined by the activity of cells in monkey dorsal premotor (PMd), primary motor (M1), and dorsolateral prefrontal cortex (dlPFC) as well as the external and internal segments of the globus pallidus (GPe, GPi). Dimensionality reduction shows that the four strongest components of neural activity are functionally interpretable, reflecting a state transition between deliberation and commitment, the transformation of sensory evidence into a choice, and the baseline and slope of the rising urgency to decide. Analysis of the contribution of each population to these components shows meaningful differences between regions but no distinct clusters within each region, consistent with an integrated dynamical system. During deliberation, cortical activity unfolds on a two-dimensional “decision manifold” defined by sensory evidence and urgency and falls off this manifold at the moment of commitment into a choice-dependent trajectory leading to movement initiation. The structure of the manifold varies between regions: In PMd, it is curved; in M1, it is nearly perfectly flat; and in dlPFC, it is almost entirely confined to the sensory evidence dimension. In contrast, pallidal activity during deliberation is primarily defined by urgency. We suggest that these findings reveal the distinct functional contributions of different brain regions to an integrated dynamical system governing action selection and execution.

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Structure in Neural Activity during Observed and Executed Movements Is Shared at the Neural Population Level, Not in Single Neurons

Cited by 39 publications

References 73 publications

Neural dynamics of causal inference in the macaque frontoparietal circuit

Neural dynamics of causal inference in the macaque frontoparietal circuit

Largely shared neural codes for biological and nonbiological observed movements but not for executed actions in monkey premotor areas

Integrated neural dynamics of sensorimotor decisions and actions

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