Agent-based representations of objects and actions in the monkey pre-supplementary motor area

Livi, Alessandro; Lanzilotto, Marco; Maranesi, Monica; Fogassi, Leonardo; Rizzolatti, Giacomo; Bonini, Luca

doi:10.1073/pnas.1810890116

Cited by 42 publications

(47 citation statements)

References 50 publications

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“…By analogy with object affordance, these resources might include the anterior pre-supplementary motor cortex (pre-SMA) that typically codes a yet unspecified readiness for action associated with the perception of affordable targets [49]. These properties of pre-SMA have been widely described by studies in non-human primates [50,51] and seem to also play an important role in social learning [52,53]. More broadly, the results of our experiments clearly indicate that Interactive gestures are processed via a different route as compared to equally salient and socially relevant gestures that do not have an affordance for motor interaction.…”

Section: Plos Onementioning

confidence: 99%

The engaging nature of interactive gestures

Curioni¹,

Knoblich²,

Sebanz³

et al. 2020

PLoS ONE

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The social interactions that we experience from early infancy often involve actions that are not strictly instrumental but engage the recipient by eliciting a (complementary) response. Interactive gestures may have privileged access to our perceptual and motor systems either because of their intrinsically engaging nature or as a result of extensive social learning. We compared these two hypotheses in a series of behavioral experiments by presenting individuals with interactive gestures that call for motor responses to complement the interaction ('hand shaking', 'requesting', 'high-five') and with communicative gestures that are equally socially relevant and salient, but do not strictly require a response from the recipient ('Ok', 'Thumbs up', 'Peace'). By means of a spatial compatibility task, we measured the interfering power of these task-irrelevant stimuli on the behavioral responses of individuals asked to respond to a target. Across three experiments, our results showed that the interactive gestures impact on response selection and reduce spatial compatibility effects as compared to the communicative (non-interactive) gestures. Importantly, this effect was independent of the activation of specific social scripts that may interfere with response selection. Overall, our results show that interactive gestures have privileged access to our perceptual and motor systems, possibly because they entail an automatic preparation to respond that involuntary engages the motor system of the observers. We discuss the implications from a developmental and neurophysiological point of view.

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Section: Plos Onementioning

confidence: 99%

The engaging nature of interactive gestures

Curioni¹,

Knoblich²,

Sebanz³

et al. 2020

PLoS ONE

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“…This shared coding of actions between the self and others has been associated with diverse roles, including intention reading via embodied simulation 5 , and is hypothesized to be deficient in autism spectrum disorder (ASD) [6][7][8] . Later work has shown, however, that the MPFC also contains neurons with mirror properties [9][10][11] . In a similar vein, it has been argued that the existence of self neurons and other neurons in the MPFC [9][10][11] may characterize its unique role in self-other distinction 12 .…”

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confidence: 99%

“…Later work has shown, however, that the MPFC also contains neurons with mirror properties [9][10][11] . In a similar vein, it has been argued that the existence of self neurons and other neurons in the MPFC [9][10][11] may characterize its unique role in self-other distinction 12 . Self neurons and other neurons are those that selectively or preferentially encode the self-action and others' action, respectively, and the paucity of other neurons in the MPFC is associated with a spontaneous autistic phenotype in a macaque monkey 13 .…”

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confidence: 99%

A causal role for frontal cortico-cortical coordination in social action monitoring

et al. 2020

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Decision-making via monitoring others’ actions is a cornerstone of interpersonal exchanges. Although the ventral premotor cortex (PMv) and the medial prefrontal cortex (MPFC) are cortical nodes in social brain networks, the two areas are rarely concurrently active in neuroimaging, inviting the hypothesis that they are functionally independent. Here we show in macaques that the ability of the MPFC to monitor others’ actions depends on input from the PMv. We found that delta-band coherence between the two areas emerged during action execution and action observation. Information flow especially in the delta band increased from the PMv to the MPFC as the biological nature of observed actions increased. Furthermore, selective blockade of the PMv-to-MPFC pathway using a double viral vector infection technique impaired the processing of observed, but not executed, actions. These findings demonstrate that coordinated activity in the PMv-to-MPFC pathway has a causal role in social action monitoring.

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“…This ability seems to rely on a network of anatomically interconnected regions ( 9 – 11 ). Indeed, view-dependent neural encoding of others’ actions has been reported in the ventral ( 12 – 14 ) and mesial ( 15 , 16 ) premotor cortex, prefrontal cortex ( 17 ), inferior parietal cortex ( 18 ), and, of course, superior temporal sulcus ( 19 , 20 ), which represents the primary source of visual information for the parietofrontal action observation network ( 21 ) via the anterior intraparietal area (AIP).…”

mentioning

confidence: 99%

Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons

Lanzilotto

Maranesi

Livi

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Humans accurately identify observed actions despite large dynamic changes in their retinal images and a variety of visual presentation formats. A large network of brain regions in primates participates in the processing of others’ actions, with the anterior intraparietal area (AIP) playing a major role in routing information about observed manipulative actions (OMAs) to the other nodes of the network. This study investigated whether the AIP also contributes to invariant coding of OMAs across different visual formats. We recorded AIP neuronal activity from two macaques while they observed videos portraying seven manipulative actions (drag, drop, grasp, push, roll, rotate, squeeze) in four visual formats. Each format resulted from the combination of two actor’s body postures (standing, sitting) and two viewpoints (lateral, frontal). Out of 297 recorded units, 38% were OMA-selective in at least one format. Robust population code for viewpoint and actor’s body posture emerged shortly after stimulus presentation, followed by OMA selectivity. Although we found no fully invariant OMA-selective neuron, we discovered a population code that allowed us to classify action exemplars irrespective of the visual format. This code depends on a multiplicative mixing of signals about OMA identity and visual format, particularly evidenced by a set of units maintaining a relatively stable OMA selectivity across formats despite considerable rescaling of their firing rate depending on the visual specificities of each format. These findings suggest that the AIP integrates format-dependent information and the visual features of others’ actions, leading to a stable readout of observed manipulative action identity.

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Agent-based representations of objects and actions in the monkey pre-supplementary motor area

Cited by 42 publications

References 50 publications

The engaging nature of interactive gestures

The engaging nature of interactive gestures

A causal role for frontal cortico-cortical coordination in social action monitoring

Stable readout of observed actions from format-dependent activity of monkey’s anterior intraparietal neurons

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