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Caramazza, A.

Publications and source records attributed to Caramazza, A..

At least 19 recordsLinked to original sources

Spatial organization of neural responses to physical and agentive movement dynamics is reflected in intrinsic functional connectivity

Making sense of dynamic scenes requires interpreting the movements of inanimate objects governed by external physical forces and the actions of animate agents pursuing endogenous goals. Prior research has identified regions preferring physical or agentive movement, but their spatial organization relative to one another remains unclear. We used fMRI and within-individual analyses to examine neural responses during a motion prediction task in which two dots moved either according to physical forces (physical condition) or in coordinated, self-propelled ways suggesting intentional action (agentive condition). Resting-state data from the same participants independently characterized functional connectivity. Preferential responses to physical and agentive movement were interdigitated across frontal, parietal, and temporal cortices. Regions sharing a preference were intrinsically connected even when widely separated, while regions with opposing preferences belonged to separate networks even when adjacent. Together, these results reveal that differences between physical and agentive dynamics are not confined to local task-evoked preferences but are embedded within the brain's broader functional organization.

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Dissociation between physical reasoning and tool use in individuals with left hemisphere brain damage

Many everyday tasks, from chopping vegetables to catching a ball, require understanding both how objects respond to physical forces and how to use them effectively. These capacities, tool use and physical reasoning, are often assumed to rely on shared cognitive and neural mechanisms. At some level, this correspondence is expected: using an object typically requires understanding its physical properties. However, both capacities are complex and multicomponential, so the relationship between them may vary across levels of representation and task demands. Here, we asked whether third-person physical reasoning about object dynamics can dissociate from tool use (i.e., performing a tools typical action, such as using a hammer to drive a nail) in individuals with left-hemisphere stroke. We tested 11 patients, five of whom showed impairments in tool use. Physical reasoning was assessed using a novel collection of tasks probing judgments about mass, velocity, and timing across static and dynamic scenes. Tool use was evaluated using a classic gesture-to-sight task, a pantomime-based measure in which participants are shown pictures of familiar tools and asked to demonstrate how each would be used. We identified an individual-level dissociation: patient I.A.* showed impairment in gesturing the use of objects despite preserved physical reasoning, often outperforming neurotypical controls. This pattern was complemented by patient N.P., who showed the reverse profile, with intact tool use gestures but difficulties in some physical reasoning tasks. These findings suggest that the ability to reason about the physical world and tool use can dissociate behaviorally and be independently disrupted by brain damage. This challenges the view that physical reasoning and tool use draw on the same underlying cognitive and neural mechanisms and suggests that at least some of their components are distinct.

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Neural representation of nouns and verbs in congenitally blind and sighted individuals

Language processing involves similar brain regions across languages and cultures. Intriguingly, one population escapes this universal pattern: in blind individuals, linguistic stimuli activate not only canonical language networks, but also the "visual" cortex. Theoretical implications of this finding are debated, particularly because it is unclear what properties of linguistic stimuli are represented in the blind visual cortex. To address this issue, we enrolled congenitally blind and sighted participants in an fMRI experiment, in which they listened to concrete, abstract, and pseudo nouns and verbs. We used multi-voxel pattern classification to investigate whether differences between nouns and verbs are represented in the blind visual cortex, and whether this effect is modulated by the words semantic category. The classification of activation patterns for nouns and verbs was above chance level in the motion-sensitive area V5/MT in the blind participants, but not in other visual areas in this group. The effect in area V5/MT was driven by successful classification of activations for concrete nouns and verbs, in the absence of significant results for abstract and pseudo nouns and verbs. These findings suggest that the blind visual cortex represents the physical properties of noun and verb referents, more salient in the concrete word category, rather than more abstract linguistic distinctions, present in all word categories. Thus, responses to language in the blind visual cortex may be explained by preserved ability of this region to compute physical and spatial representations of the world. Significance StatementIn sighted individuals, language processing involves similar brain regions across languages. Intriguingly, in blind individuals, hearing words and sentences activates not only the canonical language network, but also the "visual" cortex. What is computed in the visual cortex when blind individuals process language? Here, we show that a specific visual area in the blind - the motion-sensitive area V5/MT - responds differently to spoken nouns and verbs. We further showed that this effect is present for concrete nouns and verbs, but not for abstract or pseudo nouns and verbs. This suggests that, during language processing, the blind visual cortex represents physical features of word referents, more salient in the concrete word category, rather than more abstract linguistic distinctions, present across word categories.

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Dissociating Goal from Outcome During Action Observation

Understanding the goal of an observed action requires computing representations that are invariant to specific instantiations of the action. For example, we can accurately infer the goal of an action even when the agents desired outcome is not achieved. Observing actions consistently recruits a set of frontoparietal and posterior temporal regions, often labeled the "action observation network" (AON). While progress has been made in charting which regions of the AON, are involved in understanding goals of observed actions, it is not clear where goals are represented independently of outcomes. We used fMRI-based multivariate pattern analysis to identify such regions. Participants watched videos of successful and failed attempts of actions with different goals involving 2 different object types. We found that bilateral anterior inferior parietal lobe and right ventral premotor cortex distinguished between object-specific action goals regardless of outcomes. Left anterior inferior parietal lobe encodes action goals regardless of both outcomes and object types. Our results provide insights into the neural basis of representing action goals and the different roles of frontoparietal and posterior temporal regions in action understanding.

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The role of agentive and physical forces in the neural representation of motion events

How does the brain represent information about motion events in relation to agentive and physical forces? In this study, we investigated the neural activity patterns associated with observing animated actions of agents (e.g., an agent hitting a chair) in comparison to similar movements of inanimate objects that were either shaped solely by the physics of the scene (e.g., gravity causing an object to fall down a hill and hit a chair) or initiated by agents (e.g., a visible agent causing an object to hit a chair). Using fMRI-based multivariate pattern analysis, this design allowed testing where in the brain the neural activity patterns associated with motion events change as a function of, or are invariant to, agentive versus physical forces behind them. Cross-decoding revealed a shared neural representation of animate and inanimate motion events that is invariant to agentive or physical forces in regions spanning frontoparietal and posterior temporal cortices. In contrast, the right lateral occipitotemporal cortex showed higher sensitivity to agentive events, while the left dorsal premotor cortex was more sensitive to information about inanimate object events that were solely shaped by the physics of the scene.

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Preserved recognition of basic visual features despite lack of awareness of shape: evidence from a case of neglect

Human visual experience of objects comprises a combination of different visual features, such as their color, position, and shape. Spatial attention is thought to play a role in creating a coherent perceptual experience, integrating visual information coming from a given location, but the mechanisms underlying this process are not entirely understood. Deficits of spatial attention in which this integration process does not occur normally, such as neglect, can provide insights regarding the mechanisms of spatial attention in visual object recognition. In this study, we describe a series of experiments conducted with an individual with neglect, XX. XX presents characteristic lack of awareness of the left side of individual objects, evidenced by poor object and face recognition, and impaired word reading. However, he exhibits intact recognition of color within the boundaries of the same objects he fails to recognize. Furthermore, he can also report the orientation and location of a colored region on the neglected left side despite lack of awareness of the shape of the region. To our knowledge, selective lack of awareness of shape despite intact processing of basic visual features in the same spatial location has not been reported previously. XXs performance raises intriguing questions and challenges about the role of spatial attention in the formation of coherent object percepts and visual awareness.

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A shared neural code for the physics of actions and object events

Observing others actions recruits frontoparietal and posterior temporal brain regions - also called the action observation network. It is typically assumed that these regions support recognizing actions of animate entities (e.g., person jumping over a box). However, objects can also participate in events with rich meaning and structure (e.g., ball bouncing over a box). So far, it has not been clarified which brain regions encode information specific to goal-directed actions or more general information that also defines object events. Here, we show a shared neural code for visually presented actions and object events throughout the action observation network. We argue that this neural representation captures the structure and physics of events regardless of animacy. We find that lateral occipitotemporal cortex encodes information about events that is also invariant to stimulus modality. Our results shed light onto the representational profiles of posterior temporal and frontoparietal cortices, and their roles in encoding event information.

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The contribution of object size, manipulability, and stability on neural responses to inanimate objects

In human occipitotemporal cortex, brain responses to depicted inanimate objects have a large-scale organization by real-world object size. Critically, the size of objects in the world is systematically related to behaviorally-relevant properties: small objects are often grasped and manipulated (e.g., forks), while large objects tend to be less motor-relevant (e.g., tables), though this relationship does not always have to be true (e.g., picture frames and wheelbarrows). To determine how these two dimensions interact, we measured brain activity with functional magnetic resonance imaging while participants viewed a stimulus set of small and large objects with either low or high motor-relevance. The results revealed that the size organization was evident for objects with both low and high motor-relevance; further, a motor-relevance map was also evident across both large and small objects. Targeted contrasts revealed that typical combinations (small motor-relevant vs. large non-motor-relevant) yielded more robust topographies than the atypical covariance contrast (small non-motor-relevant vs. large motor-relevant). In subsequent exploratory analyses, a factor analysis revealed that the construct of motor-relevance was better explained by two underlying factors: one more related to manipulability, and the other to whether an object moves or is stable. The factor related to manipulability better explained responses in lateral small-object preferring regions, while the factor related to object stability (lack of movement) better explained responses in ventromedial large-object preferring regions. Taken together, these results reveal that the structure of neural responses to objects of different sizes further reflect behavior-relevant properties of manipulability and stability, and contribute to a deeper understanding of some of the factors that help the large-scale organization of object representation in high-level visual cortex. Highlights- Examined the relationship between real-world size and motor-relevant properties in the structure of responses to inanimate objects. - Large scale topography was more robust for contrast that followed natural covariance of small motor-relevant vs. large non-motor-relevant, over contrast that went against natural covariance. - Factor analysis revealed that manipulability and stability were, respectively, better explanatory predictors of responses in small- and large-object regions.

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Preference for animate domain sounds in the fusiform gyrus of blind individuals is modulated by shape-action mapping transparency

In high-level visual shape areas in the human brain, preference for inanimate objects is observed regardless of stimulation modality (visual/auditory/tactile) and subjects visual experience (sighted/blind individuals), whereas preference for animate entities seems robust only in the visual modality. Here, we test a hypothesis explaining this effect: visual shape representations can be reliably activated through different sensory modalities when they are systematically related to action system representations. We studied fMRI activations in congenitally blind and sighted subjects listening to animal, object, and human sounds. We found that, in blind individuals, the typical anatomical location of the fusiform face area responds to human facial expression sounds, with a clear mapping between the facial motor action and the resulting face shape, but not to speech or animal sounds. Using face areas activation in the blind subjects we could distinguish between specific facial expressions used in the study, but not between specific speech sounds. We conclude that auditory stimulation can reliably activate visual representations of those stimuli - inanimate or animate - for which shape and action computations are transparently related. Our study suggests that visual experience is not necessary for the development of functional preference for face-related information in the fusiform gyrus.

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Typical lipreading and audiovisual speech perception without motor simulation

All it takes is a face to face conversation in a noisy environment to realize that viewing a speakers lip movements contributes to speech comprehension. Following the finding that brain areas that control speech production are also recruited during lip reading, the received explanation is that lipreading operates through a covert unconscious imitation of the observed speech movements in the observers own speech motor system - a motor simulation. However, motor effects during lipreading do not necessarily imply simulation or a causal role in perception. In line with this alternative, we report here that some individuals born with lip paralysis, who are therefore unable to covertly imitate observed lip movements, have typical lipreading abilities and audiovisual speech perception. This constitutes existence proof that typically efficient lipreading abilities can be achieved without motor simulation. Although it remains an open question whether this conclusion generalizes to typically developed participants, these findings demonstrate that alternatives to motor simulation theories are plausible and invite the conclusion that lip-reading does not involve motor simulation. Beyond its theoretical significance in the field of speech perception, this finding also calls for a re-examination of the more general hypothesis that motor simulation underlies action perception and interpretation developed in the frameworks of the motor simulation and mirror neuron hypotheses.

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Shape-centered representations of bounded regions of space mediate the transformation of retinotopic representations into conscious perception of objects

The primary visual cortex represents the retinotopic orientation of visual primitives (edges, blobs, bars), but our conscious perception is of orientated objects (e.g., dogs, forks) in the environment. How this transformation operates remains unknown. We report here the study of a young woman presenting with an extraordinarily clear and informative visual disorder that affects highly specific aspects of object perception allowing precise inferences about the type and properties of visual representations that mediate this transformation. Davida perceives sharp-edged 2D bounded regions of space of medium to high contrast as if they were plane-rotated by 90, 180 or 270 degrees around their center, mirrored across their own axes, or both. In contrast, her perception of strongly blurred or very low contrast shapes, and of compound shapes emerging from a collection of bounded elements, is intact. The nature of her errors implies that visual perception is mediated by a representation of each bounded region of space in a shape-centered coordinate system aligned on either the shapes most elongated part or on the shapes axis of symmetry and centered either at the midpoint of the shapes most elongated part or at the shapes centroid. The selectivity of her disorder to sharp-edged medium to high-contrast stimuli additionally suggests that duplicate shape-centered representations are computed in parallel from information derived from the parvocellular and magnocellular subcortical channels and integrated precisely at the level at which shape representations must be mapped onto a behaviorally relevant frame of reference.

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Lateral occipitotemporal cortex encodes perceptual components of social actions rather than abstract representations of sociality

Neuroimaging studies suggest that areas in the lateral occipitotemporal cortex (LOTC) play an important role in the perception of social actions. However, it is unclear what precisely about social actions these areas represent: perceptual features that may be indicative of social actions - such as the presence of persons in a scene, their orientation toward each other, and in particular the directedness of action movements toward persons or other targets - or more abstract representations that capture whether an action is meant to be social. In two fMRI experiments, we used representational similarity analysis (RSA) to test whether LOTC is sensitive to perceptual action components important for social interpretation and/or more general representations of sociality (Experiment 1) and implied person-directedness (Experiment 2). We found that LOTC is sensitive to perceptual action components (person presence, person orientation, and action directedness toward different types of recipients). By contrast, more general levels of sociality and implied person-directedness were not captured by LOTC. Our findings suggest that regions in LOTC provide the perceptual basis for social action interpretation but challenge accounts that posit specialization at more general levels sensitive to social actions and sociality as such. We propose that the interpretation of an action - in terms of sociality or other intentional aspects - arises from the interaction of multiple areas in processing relevant action components in a situation-dependent manner.

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Individuation of parts of a single object and multiple distinct objects relies on a common neural mechanism in inferior intraparietal sulcus

Object identification and enumeration rely on the ability to distinguish, or individuate, objects from the background. Does multiple object individuation operate only over bounded, separable objects or does it operate equally over connected features within a single object? While previous fMRI experiments suggest that connectedness affects the processing and enumeration of objects, recent behavioral and EEG studies demonstrated that parallel individuation occurs over both object parts and distinct objects. However, it is unclear whether individuation of object parts and distinct objects relies on a common or independent neural mechanisms. Using fMRI-based multivariate pattern analyses, we here demonstrate that activity patterns in inferior and superior intraparietal sulci (IPS) encode numerosity independently of whether the individuated items are connected parts of a single object or distinct objects. Lateral occipital cortex is more sensitive to perceptual aspects of the two stimulus types and the targets of the stimuli, suggesting a dissociation between ventral and dorsal areas in representing perceptual object properties and more general information about numerosity, respectively. Our results suggest that objecthood is not a necessary prerequisite for parallel individuation in IPS. Rather, our results point toward a common individuation mechanism that selects targets over a flexible object hierarchy, independently of whether the targets are distinct separable objects or parts of a single object.

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Two Forms of Knowledge Representations in the Human Brain

Sensory experience shapes what and how knowledge is stored in the brain -- our knowledge about the color of roses depends in part on the activity of color-responsive neurons based on experiences of seeing roses. We study the brain basis of color knowledge in congenitally blind individuals whose color knowledge can only be obtained through language descriptions. We found that some regions support color knowledge only in the sighted. More importantly, a region in the left dorsal anterior temporal lobe supports object color knowledge in both the blind and sighted groups, indicating the existence of a sensory-independent knowledge coding system in both groups. Thus, there are (at least) two forms of object knowledge representations in the human brain: sensory-derived and cognitively-derived knowledge, supported by different brain systems.

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Representation of action concepts in left posterior temporal cortex that generalize across vision and language

Both temporal and frontoparietal brain areas are associated with the representation of knowledge about the world, in particular about actions. However, what these brain regions represent and precisely how they differ remains unknown. Here, we reveal fundamentally distinct functional profiles of lateral temporal and frontoparietal cortex: Using fMRI-based MVPA we found that frontoparietal areas encode representations of observed actions and corresponding written sentences in an overlapping way, but these representations did not generalize across stimulus type. By contrast, only left lateral posterior temporal cortex (LPTC) encoded action representations that generalize across observed action scenes and sentences. The representational organization of stimulus-general action information in LPTC could be predicted from models that describe basic agent-patient relations (object- and person-directedness) and the general semantic similarity between actions. The match between action videos and sentences in LPTC and its representational profile indicate that this region encodes general, conceptual aspects of actions whereas frontoparietal representations appear to be tied to specific stimulus types.

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Large-scale organization of the hand action observation network in individuals born without hands

The human high-level visual cortex comprises regions specialized for the processing of distinct types of stimuli, such as objects, animals, and human actions. How does this specialization emerge? Here, we investigated the role of sensorimotor experience in shaping the organization of the action observation network as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g. during monitoring ones own movements and imitation, resulting in bidirectionally connected circuits between areas involved in body movements observation (e.g., of the hand) and the motor codes involved in their execution. If the organization of the action observation network is shaped by this sensorimotor coupling, then, it should not form for body movements that do not belong to individuals motor repertoire. To test this prediction, we used fMRI to investigate the spatial arrangement and functional properties of the hand and foot action observation circuits in individuals born without upper limbs. Multivoxel pattern decoding, pattern similarity, and univariate analyses revealed an intact hand action observation network in the individuals born without upper limbs. This suggests that the organization of the action observation network does not require effector-specific visuomotor coupling.

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How do blind people represent rainbows? Disentangling components of conceptual representations.

How do we represent information that has no sensory features? How are abstract concepts like \"freedom\", devoid of external perceptible referents, represented in the brain? To address the role of sensory information in the neural representation of concepts, we investigated how people born blind process concepts whose referents are imperceptible to them because of their visual nature (e.g. \"rainbow\", or \"red\"). We find that the left dorsal anterior temporal lobe (ATL) shows preference both to typical abstract concepts (\"freedom\") and to concepts whose referents are not sensorially-available to the blind (\"rainbow\"), as compared to partially sensorially-perceptible referents (e.g. \"rain\"). Activation pattern similarity in dorsal ATL is related to the sensorial-accessibility ratings of the concepts in the blind. Parts of inferior-lateral aspects of ATL and the temporal pole responded preferentially to abstract concepts devoid of any external referents (\"freedom\") relative to imperceptible objects, in effect distinguishing between object and non-object concepts. The medial ATL showed a preference for concrete concepts (\"cup\"), along with a preference for partly perceptible items to the blind (\"rain\", as compared with \"rainbow\"), indicating this regions role in representing concepts with sensory referents beyond vision. The findings point to a new division of labor among medial, dorsal and lateral aspects of ATL in representing different properties of object and non-object concepts.

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Limitations of compensatory plasticity: the organization of the primary sensorimotor cortex in foot-using bilateral upper limb dysplasics

What forces direct brain organization and its plasticity? When a brain region is deprived of its input would this region reorganize based on compensation for the disability and experience, or would strong limitations of brain structure limit its plasticity? People born without hands activate their sensorimotor hand region while moving body parts used to compensate for this ability (e.g. their feet). This has been taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts. Here we test the selectivity for functionally-compensatory body parts in the sensorimotor cortex of people born without hands. Despite clear compensatory foot use, the sensorimotor hand area in the dysplasic subjects showed preference for body parts whose cortical territory is close to the hand area, but which are not compensatorily used as effectors. This suggests that function-based organization, originally proposed for congenital blindness and deafness, does not apply to cases of the primary sensorimotor cortex deprivation in dysplasia. This is consistent with the idea that experience-independent functional specialization occurs at relatively high levels of representation. Indeed, increased and selective foot movement preference in the dysplasics was found in the association cortex, in the inferior parietal lobule. Furthermore, it stresses the roles of neuroanatomical constraints such as topographical proximity and connectivity in determining the functional development of brain regions. These findings reveal limitations to brain plasticity and to the role of experience in shaping the functional organization of the brain.\n\nSignificance StatementWhat determines the role of brain regions, and their plasticity when typical inputs or experience is not provided? To what extent can extreme compensatory use affect brain organization? We tested the functional reorganization of the primary sensorimotor cortex hand area in people born without hands, who use their feet for every-day tasks. We found that it is preferentially activated by close-by body-parts which cannot serve as effectors, and not by the feet. In contrast, foot-selective compensatory plasticity was found in the association cortex, in an area involved in tool use. This shows limitations of compensatory plasticity and experience in modifying brain organization of early topographical cortex, as compared to association cortices where function-based organization is the driving factor.\n\nClassificationBiological Sciences\\Neuroscience

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