Differential neural dynamics underlying pragmatic and semantic affordance processing in macaque ventral premotor cortex

Maranesi, Monica; Bruni, Stefania; Livi, Alessandro; Rigoli, Francesco; Pezzulo, Giovanni; Bonini, Luca

doi:10.1038/s41598-019-48216-y

Cited by 7 publications

(5 citation statements)

References 51 publications

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“…The concept of affordances refers to the action possibilities of the environment that are available to an animal: 'the affordances of the environment are what it offers the animal, what it provides or furnishes, either for good or ill' [13]. Gibson introduced this concept to overcome the classical dichotomy between perception and action, but most of extant studies have exclusively focused on the investigation of object affordances [51,[90][91][92][93][94].…”

Section: Box 1 Extending the Concept Of Affordancesmentioning

confidence: 99%

From Observed Action Identity to Social Affordances

Orban

Lanzilotto

Bonini

2021

Trends in Cognitive Sciences

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Others' observed actions cause continuously changing retinal images, making it challenging to build neural representations of action identity. The monkey anterior intraparietal area (AIP) and its putative human homologue (phAIP) host neurons selective for observed manipulative actions (OMAs). The neuronal activity of both AIP and phAIP allows a stable readout of OMA identity across visual formats, but human neurons exhibit greater invariance and generalize from observed actions to action verbs. These properties stem from the convergence in AIP of superior temporal signals concerning: (i) observed body movements; and (ii) the changes in the body-object relationship. We propose that evolutionarily preserved mechanisms underlie the specification of observed-actions identity and the selection of motor responses afforded by them, thereby promoting social behavior. Combining Observed Body Movements and Objects Changes: The Action's IdentityManual skills are a hallmark of primates, particularly humans. They have made possible most of our transformational impact on the world, which was driven by an evolutionarily preserved but expanding network of cortical areas in the primate lineage that subserves the neural control of manipulative actions [1][2][3][4]. Interestingly, an equally well-articulated neural machinery is required to resolve the visual complexity of observed manipulative actions (OMAs) (see Glossary) performed by other individuals, because this ability is of critical importance for action planning during social interaction and interindividual coordination [5][6][7]. Indeed, as compared with other complex static visual stimuli, such as objects [8], faces [9,10], others' gaze direction [11], and body posture [12], observed actions of others are inherently dynamic stimuli, and their dynamics are essential for an observer's brain to compute their identity, despite the rapid changes in their retinal image. This is probably the reason why James Gibson claimed that 'animals are by far the most complex objects of perception that the environment presents to an observer' [13].

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Section: Box 1 Extending the Concept Of Affordancesmentioning

confidence: 99%

From Observed Action Identity to Social Affordances

Orban

Lanzilotto

Bonini

2021

Trends in Cognitive Sciences

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“…However, color, glossiness and 3D texture, as well as other visual signals about material properties of objects, provide important clues about their behavioral relevance. For example, the ripeness or palatability of a fruit suggests what to do with it (Bruni et al 2017 ; Maranesi et al 2019 ). These properties concern the physical appearance of objects, thereby conveying “semantic” information in addition to the pragmatic description.…”

Section: Visual and Haptic Signals For Manipulative-action Planningmentioning

confidence: 99%

Parietal maps of visual signals for bodily action planning

2021

Self Cite

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The posterior parietal cortex (PPC) has long been understood as a high-level integrative station for computing motor commands for the body based on sensory (i.e., mostly tactile and visual) input from the outside world. In the last decade, accumulating evidence has shown that the parietal areas not only extract the pragmatic features of manipulable objects, but also subserve sensorimotor processing of others’ actions. A paradigmatic case is that of the anterior intraparietal area (AIP), which encodes the identity of observed manipulative actions that afford potential motor actions the observer could perform in response to them. On these bases, we propose an AIP manipulative action-based template of the general planning functions of the PPC and review existing evidence supporting the extension of this model to other PPC regions and to a wider set of actions: defensive and locomotor actions. In our model, a hallmark of PPC functioning is the processing of information about the physical and social world to encode potential bodily actions appropriate for the current context. We further extend the model to actions performed with man-made objects (e.g., tools) and artifacts, because they become integral parts of the subject’s body schema and motor repertoire. Finally, we conclude that existing evidence supports a generally conserved neural circuitry that transforms integrated sensory signals into the variety of bodily actions that primates are capable of preparing and performing to interact with their physical and social world.

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“…No such effect was found if the object was out of reach, either because located at 1.5 m from the participant (Costantini et al 2010 ; Exp1) or behind a semi-opaque screen (ibid., Exp2). Distance-related effects were also reported in a behavioral study using object pictures as primes for action verbs (Costantini et al 2011 ), and in animal experiments recording object-triggered responses from premotor neurons, which showed similar space-constrained modulation (Bonini et al 2014 ; Maranesi et al 2014 ) as well as different dynamics based on the context in which objects are presented (Maranesi et al 2019 ). A possible account for these contrasting findings has been proposed (Borghi and Riggio 2009 , 2015 ) whereby a distinction is made between stable and variable affordances.…”

Section: Introductionmentioning

confidence: 67%

Do graspable objects always leave a motor signature? A study on memory traces

Daprati

Balestrucci²,

Nico

2022

Exp Brain Res

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Several studies have reported the existence of reciprocal interactions between the type of motor activity physically performed on objects and the conceptual knowledge that is retained of them. Whether covert motor activity plays a similar effect is less clear. Certainly, objects are strong triggers for actions, and motor components can make the associated concepts more memorable. However, addition of an action-related memory trace may not always be automatic and could rather depend on ‘how’ objects are encountered. To test this hypothesis, we compared memory for objects that passive observers experienced as verbal labels (the word describing them), visual images (color photographs) and actions (pantomimes of object use). We predicted that the more direct the involvement of action-related representations the more effective would be the addition of a motor code to the experience and the more accurate would be the recall. Results showed that memory for objects presented as words i.e., a format that might only indirectly prime the sensorimotor system, was generally less accurate compared to memory for objects presented as photographs or pantomimes, which are more likely to directly elicit motor simulation processes. In addition, free recall of objects experienced as pantomimes was more accurate when these items afforded actions performed towards one’s body than actions directed away from the body. We propose that covert motor activity can contribute to objects’ memory, but the beneficial addition of a motor code to the experience is not necessarily automatic. An advantage is more likely to emerge when the observer is induced to take a first-person stance during the encoding phase, as may happen for objects affording actions directed towards the body, which obviously carry more relevance for the actor.

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Differential neural dynamics underlying pragmatic and semantic affordance processing in macaque ventral premotor cortex

Cited by 7 publications

References 51 publications

From Observed Action Identity to Social Affordances

From Observed Action Identity to Social Affordances

Parietal maps of visual signals for bodily action planning

Do graspable objects always leave a motor signature? A study on memory traces

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