From Observed Action Identity to Social Affordances

نویسندگان

چکیده

A substantial fraction of neurons in the monkey anterior intraparietal area (AIP) and its human homologue phAIP are selective for observed manipulative actions (OMAs).OMA encode identity actions, up to level semantic representation phAIP.OMA may result from combination two visual signals originating superior temporal sulcus (STS) concerning: (i) body movements: (ii) changes hand/object relationship (action effects).Others’ beyond grasping, be specified parietal territories, underpinning ‘social affordance’ processing selection potential behavioral responses parieto-premotor circuits. Others’ cause continuously changing retinal images, making it challenging build neural representations action identity. The putative (phAIP) host (OMAs). neuronal activity both AIP allows a stable readout OMA across formats, but exhibit greater invariance generalize verbs. These properties stem convergence movements; body–object relationship. We propose that evolutionarily preserved mechanisms underlie specification observed-actions motor afforded by them, thereby promoting social behavior. Manual skills hallmark primates, particularly humans. They have made possible most our transformational impact on world, which was driven an expanding network cortical areas primate lineage subserves control [1.Padberg J. et al.Parallel evolution involved skilled hand use.J. Neurosci. 2007; 27: 10106-10115Crossref PubMed Scopus (111) Google Scholar, 2.Kaas J.H. Stepniewska I. Evolution posterior cortex parietal-frontal networks specific primates.J. Comp. Neurol. 2016; 524: 595-608Crossref (53) 3.Borra E. al.The macaque lateral grasping network: substrate generating purposeful actions.Neurosci. Biobehav. Rev. 2017; 75: 65-90Crossref (54) 4.Goldring A.B. Krubitzer L.A. Chapter 26 - mammals: manipulation tool use.in: Kaas Evolutionary Neuroscience. Second Edition. Academic Press, 2020: 627-656Crossref Scholar]. Interestingly, equally well-articulated machinery is required resolve complexity (OMAs) (see Glossary) performed other individuals, because this ability critical importance planning during interaction interindividual coordination [5.Lanzilotto M. al.Neuronal encoding self others’ head rotation dorsal prefrontal cortex.Sci. Rep. 7: 8571Crossref (7) 6.Sacheli L.M. al.How task interactivity shapes observation.Cereb. Cortex. 2019; 29: 5302-5314Crossref (5) 7.Ninomiya T. al.A causal role frontal cortico–cortical monitoring.Nat. Commun. 2020; 11: 5233Crossref (1) Indeed, as compared with complex static stimuli, such objects [8.Bao P. map object space inferotemporal cortex.Nature. 583: 103-108Crossref (19) Scholar], faces [9.Chang L. Tsao D.Y. code facial brain.Cell. 169: 1013-1028.e14Abstract Full Text PDF (190) Scholar,10.Freiwald W.A. face processing: cells, areas, networks, models.Curr. Opin. Neurobiol. 60: 184-191Crossref (4) gaze direction [11.Shepherd S.V. al.Mirroring attention cortex.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 9489-9494Crossref (93) posture [12.Kumar al.Transformation ventral stream body-selective patches.Cereb. 215-229Crossref (8) others inherently dynamic their dynamics essential observer’s brain compute identity, despite rapid image. This probably reason why James Gibson claimed ‘animals far perception environment presents observer’ [13.Gibson J.J. Ecological Approach Visual Perception. Houghton Mifflin, 1979Google Body movements fundamental component ‘action’; nonetheless, they represent only one component. In fact, much more than set coordinated movements, since aims produce change subject immersed [14.Bonini al.Neurophysiological bases underlying organization intentional understanding intention.Conscious. Cogn. 2013; 22: 1095-1104Crossref (24) Thus, agent’s causes target constitute element almost important movement itself, make predictable terms goal [15.Oram M.W. Perrett D.I. Integration form motion polysensory (STPa) monkey.J. Neurophysiol. 1996; 76: 109-129Crossref (283) 16.Kilner J.M. al.Motor activation prior observation predicted movement.Nat. 2004; 1299-1301Crossref 17.Maranesi al.Mirror neuron context.J. 2014; 34: 14827-14832Crossref (43) types signal, specifying: how unfold; will position or shape object, naturally coexist everyday characterize Both elements crucial. For example, same act branch serve secure while climbing, manipulate grabbing fruits, use hit something someone else: spite body-movement similarity, these clearly different consequences. Similarly, effect moving away can achieved pushing it, throwing kicking similar consequence outside world. Here, we first review evidence signatures OMA-identity coding brain, point node function. then elucidate connectional architecture enables integration main sources information needed identity: hand–object-interaction (i.e., attainment goal). Finally, extension model larger variety classes ones addition AIP, should drive future studies computation non-human brain. Area has long been considered crucial system routing regarding 3D [18.Murata al.Selectivity shape, size, orientation AIP.J. 2000; 83: 2580-2601Crossref 19.Verhoef B.-E. al.Effects microstimulation three-dimensional Categorization.PLoS One. 2015; 10e0136543Crossref (11) 20.Schaffelhofer Scherberger H. Object vision parietal, premotor, cortices.eLife. 5e15278Crossref (47) Scholar] [21.Pani al.Grasping execution single area.J. 26: 2342-2355Crossref (45) Scholar,22.Maeda K. al.Functional manipulation-related mirror responding own action.J. 560-572Crossref (40) [23.Perrett al.Frameworks analysis animate actions.J. Exp. Biol. 1989; 146: 87-113Crossref Scholar,24.Singer Sheinberg D.L. Temporal articulated slow sequences integrated poses.J. 2010; 30: 3133-3145Crossref (0) [25.Gamberini al.Sensory caudal aspect macaque’s lobule.Brain Struct. Funct. 2018; 223: 1863-1879PubMed Scholar,26.Breveglieri R. al.Neurons modulated medial cortex.Curr. 1218-1225.e3Abstract (6) regions premotor [27.Maranesi al.Cortical affordances action.Front. Psychol. 5: 538Crossref whereas neighboring inferior convexity were deemed play other’s [28.Rozzi lobule monkey: electrophysiological characterization motor, sensory, correlation cytoarchitectonic areas.Eur. 2008; 28: 1569-1588Crossref Scholar,29.Rizzolatti G. goal-directed neuron-based understanding.Physiol. 94: 655-706Crossref (239) Extant focused exclusively graspable exception recent investigations recorded monkeys exemplars [30.Lanzilotto al.Anterior area: hub network.Cereb. 1816-1833Crossref (16) Scholar,31.Lanzilotto al.Stable format-dependent monkey’s neurons.Proc. 117: 16596-16605Crossref (3) findings latter demonstrate about OMAs nodes network. What through achieve actions? study [31.Lanzilotto displayed marked selectivity another grooming) among including emotional gestures lip smacking screaming), neutral yawning chewing), stimuli still monkey, animal, landscape) presented screen. study, also tested large dragging, dropping, pulling, pushing, rotating, squeezing) previously used reveal action-identity addition, four resulting postures actor (standing sitting) viewpoints (lateral frontal) (Figure 1A ). results showed 38% at least format, distinct sets exhibiting preference exemplar (or exemplars), tuning presentation format example Figure 1A). However, no fully visual-invariant found. dynamically according multiplicative mixing described images [32.Ratan Murty N.A. Arun S.P. Multiplicative image attributes 115: E3276-E3285Crossref Such decoding early signal viewpoint (50 ms after stimulus onset) actor’s (at 100 ms) and, slightly later (150 ms), even format-independent manner. Crucially, accuracy decoded depends upon presence subset units maintain relatively formats considerable rescaling firing rate specificities each (as relationship, if exists, between individual AIP? clustering indicated characterized toward lying table (e.g., dragging) closely linked consequently, segregated those already contact manipulated rolling squeezing, 1B). largely independent combinations 1C), suggesting relationships contribution 1A) recently patients participating brain–machine interface clinical trial, allowing researchers record single-neuron rostral [33.Aflalo shared verbs Adv. 6eabb3984Crossref region include [34.Orban G.A. Functional definitions primates.Proc. 283: 1828Google revealed impressive similarities reported monkeys. First, viewpoint, approximately 20% selective, majority them facilitated response 1D), smaller (about 15%) suppressed humans Second, could tuned any tested, coverage uniform Third, population patients, providing significant latency video onset). evident neurons, although difficult reach firm conclusion based available evidence, plausible common ancestor differently sizable OMA-selective exhibited format-invariant (80% invariant 55% invariant), consistent generalization OMA-discrimination tasks [35.Platonov Orban Action observation: less-explored part higher-order vision.Sci. 6: 36742Crossref thus facilitate recruitment reading uniquely capacity. To summarize, primates macaques) remarkably sulcus, variable degree abstraction order access via written words functional basic raise question what anatomical might be. prevalent portion where influence own-hand feedback overall responsiveness found stronger sector tracers injected three positions along rostro-caudal extent physiologically investigated region. confirmed previous [36.Borra connections area.Cereb. 18: 1094-1111Crossref (302) 2A ) quantitative differences connectivity patterns 2B). particular, selectivity, regions, area, occipito-temporal 2C). Although yet neurophysiological lower bank (STS), known target. discharge when isolation some distance other. Furthermore, STS responded similarly many [22.Maeda Scholar,30.Lanzilotto Scholar]; enable assess consequences hand–object interactions. Importantly, unaffected except rigidity food quality. resulted effects essentially rather itself. location corresponds TEa [37.Seltzer B. Pandya D.N. Afferent architectonics surrounding rhesus monkey.Brain Res. 1978; 149: 1-24Crossref (575) prominent projection targeting mainly part, prevail TEa–AIP pathway (red arrow 2C) likely represents source manipulations. Areas IPa/PGa potentially relevant targeted middle-STS [38.Vangeneugden differentiation using parametric space.Cereb. 19: 593-611Crossref (75) features forelimb portrayed stick figures: body-part deformation, encoded ‘snapshot’ kinematic features, ‘motion’ neurons. cells provide rich extracting interactions [39.Sliwa Freiwald dedicated brain.Science. 356: 745-749Crossref (85) Scholar,40.Ong W.S. correlates strategic cooperation monkeys.Nat. 2021; 24: 116-128Crossref constituting key proposed ‘third pathway’ [41.Pitcher D. Ungerleider L.G. Evidence third specialized perception.Trends 25: 100-110Abstract (2) Thus far, there little view independence body-patch display mostly view-dependent line (such walking bending knee) [42.Jellema Neural perceived bodily categorical frame reference.Neuropsychologia. 2006; 44: 1535-1546Crossref (blue 2C), coherently strong anatomo-functional reviewed preceding text suggests receives convergent 3, Key Figure): TEa. Considering homology [43.Jastorff al.Integration cues biological STS.Neuroimage. 2012; 911-921Crossref scheme extended located occipitotemporal extends into fusiform gyrus Scholar]: contribute caused [44.Wurm M.F. Caramazza Lateral encodes perceptual components abstract sociality.Neuroimage. 202116153Crossref By contrast, split middle gyrus, extend correspond activations [45.Beauchamp M.S. streams manipulable movements.Neuron. 2002; 149-159Abstract (409) Scholar,46.Jastorff Human magnetic resonance imaging reveals separation processing.J. 7315-7329Crossref Why represented primates’ cortex? As mentioned previously, monkeys, show either responses; however, active reaching–grasping dark, (not ones) genuine response. On basis, visuomotor doing. mechanism would work alongside affordances. physical Scholar,21.Pani [20.Schaffelhofer Scholar,47.Jeannerod objects: transformation.Trends 1995; 314-320Abstract (1029) Scholar,48.Bonini al.Space-dependent neurons.J. 4108-4119Crossref (67) forming parieto-frontal circuit experimentally established visually guided [49.Gallese V. al.Deficit preshaping muscimol injection cortex.Neuroreport.

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ژورنال

عنوان ژورنال: Trends in Cognitive Sciences

سال: 2021

ISSN: ['1364-6613', '1879-307X']

DOI: https://doi.org/10.1016/j.tics.2021.02.012