Vannuscorps, G., Wurm, M. F., Striem-Amit, E., & Caramazza, A. (2018). Large-scale organizations of the hand action observation network in individuals born without hands. Cerebral Cortex.Abstract
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 effector-specific visuomotor coupling experience in shaping the organization of the action observation network (AON) as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g., during monitoring one’s 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 AON is shaped by this effector-specific visuomotor 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 AON in the individuals born without upper limbs. This suggests that the organization of the AON does not require effector-specific visuomotor coupling.
Striem-Amit, E., Vannuscorps, G., & Caramazza, A. (2018). Plasticity based on compensatory effector use in the association but not primary sensorimotor cortex of people born without hands. Proceedings of the National Academy of Sciences , 115 (30), 7801-7806.Abstract
What forces direct brain organization and its plasticity? When brain regions are deprived of their input, which regions reorganize based on compensation for the disability and experience, and which regions show topographically constrained plasticity? People born without hands activate their primary sensorimotor hand region while moving body parts used to compensate for this disability (e.g., their feet). This was taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts, in primary sensorimotor cortex. We tested the selectivity for the compensatory body parts in the primary and association sensorimotor cortex of people born without hands (dysplasic individuals). Despite clear compensatory foot use, the primary sensorimotor hand area in the dysplasic subjects showed preference for adjacent body parts that are not compensatorily used as effectors. This suggests that function-based organization, proposed for congenital blindness and deafness, does not apply to the primary sensorimotor cortex deprivation in dysplasia. These findings stress the roles of neuroanatomical constraints like topographical proximity and connectivity in determining the functional development of primary cortex even in extreme, congenital deprivation. In contrast, increased and selective foot movement preference was found in dysplasics’ association cortex in the inferior parietal lobule. This suggests that the typical motor selectivity of this region for manual actions may correspond to high-level action representations that are effector-invariant. These findings reveal limitations to compensatory plasticity and experience in modifying brain organization of early topographical cortex compared with association cortices driven by function-based organization.
Bracci, S., Caramazza, A., & Peelen, M. V. (2018). View-invariant representation of hand postures in the human lateral occipitotemporal cortex. NeuroImage , 181, 446-452.Abstract
Understanding other people's actions and mental states includes the interpretation of body postures and movements. In particular, hand postures are an important channel to signal both action and communicative intentions. Recognizing hand postures is computationally challenging because hand postures often differ only in the subtle configuration of relative finger positions and because visual characteristics of hand postures change across viewpoints. To allow for accurate interpretation, the brain needs to represent hand postures in a view-invariant but posture-specific manner. Here we test for such representations in hand-, body-, and object-selective regions of the lateral occipitotemporal cortex (LOTC). We used multivariate pattern analysis of fMRI data to test for view-specific and view-invariant representations of individual hand postures, separately for two domains: action-related postures (e.g., a precision grasp) and communicative postures (e.g., thumbs up). Results showed that hand-selective LOTC, but not nearby body- and object-selective LOTC, represented hand postures in a view-invariant manner, with relatively similar activity patterns to the same hand posture seen from different viewpoints. View invariance was equally strong for action and communicative postures. By contrast, object-selective cortex represented hand postures in a view-specific manner. These results indicate a role for hand-selective LOTC in solving the view-invariance problem for individual hand postures. View-invariant representations of hand postures in this region may then be accessed and further interpreted by multiple downstream systems to inform high-level judgments related to action understanding, emotion recognition, and non-verbal communication.
Papeo, L., Wurm, M. F., Oosterhof, N. N., & Caramazza, A. (2017). The neural representation of human versus nonhuman bipeds and quadrupeds . Scientific Reports , 7 (1), 14040.Abstract
How do humans recognize humans among other creatures? Recent studies suggest that a preference for conspecifics may emerge already in perceptual processing, in regions such as the right posterior superior temporal sulcus (pSTS), implicated in visual perception of biological motion. In the current functional MRI study, participants viewed point-light displays of human and nonhuman creatures moving in their typical bipedal (man and chicken) or quadrupedal mode (crawling-baby and cat). Stronger activity for man and chicken versus baby and cat was found in the right pSTS responsive to biological motion. The novel effect of pedalism suggests that, if right pSTS contributes to recognizing of conspecifics, it does so by detecting perceptual features (e.g. bipedal motion) that reliably correlate with their appearance. A searchlight multivariate pattern analysis could decode humans and nonhumans across pedalism in the left pSTS and bilateral posterior cingulate cortex. This result implies a categorical human-nonhuman distinction, independent from within-category physical/perceptual variation. Thus, recognizing conspecifics involves visual classification based on perceptual features that most frequently co-occur with humans, such as bipedalism, and retrieval of information that determines category membership above and beyond visual appearance. The current findings show that these processes are at work in separate brain networks.
Anzellotti, S., & Caramazza, A. (2017). Multimodal representations of person identity individuated with fMRI. Cortex , 89, 85-97.
Leshinskaya, A., Contreras, J. M., Caramazza, A., & Mitchell, J. P. (2017). Neural Representations of Belief Concepts: A Representational Similarity Approach to Social Semantics. Cerebral Cortex , 27 (1), 344-357.
Wurm, M. F., Caramazza, A., & Lingnau, A. (2017). Action categories in lateral occipitotemporal cortex are organized along sociality and transitivity. Journal of Neuroscience , 37 (3), 562-575.
Striem-Amit, E., Vannuscorps, G., & Caramazza, A. (2017). Sensorimotor-independent development of hands and tools selectivity in the visual cortex. Proceedings of the National Academy of Sciences , 114 (18), 4787-4792.
Wang, X., He, C., Peelen, M. V., Gong, G., Caramazza, A., & Bi, Y. (2017). Domain selectivity in the parahippocampal gyrus is predicted by the same structural connectivity patterns in blind and sighted individuals. Journal of Neuroscience , 37 (18), 4705-4716.
Vannuscorps, G., & Caramazza, A. (2016). Typical predictive eye movements during action observation without effector-specific motor simulation. Psychonomic Bulletin & Review , 1-6.
Leshinskaya, A., & Caramazza, A. (2016). For a cognitive neuroscience of concepts: Moving beyond the grounding issue. Psychonomic Bulletin & Review , 1-11. Full TextAbstract

Cognitive neuroscience research on conceptual knowledge often is discussed with respect to “embodiment” or “grounding.” We tried to disentangle at least three distinct claims made using these terms. One of these, the view that concepts are entirely reducible to sensory-motor representations, is untenable and diminishing in the literature. A second is the view that concepts and sensory-motor representations “interact,” and a third view addresses the question of how concepts are neurally organized—the neural partitions among concepts of different kinds, and where these partitions are localized in cortex. We argue that towards the second and third issues, much fruitful research can be pursued, but that no position on them is specifically related to “grounding.” Furthermore, to move forward on them, it is important to precisely distinguish different kinds of representations—conceptual vs. sensory-motor—from each other theoretically and empirically. Neuroimaging evidence often lacks such specificity. We take an approach that distinguishes conceptual from sensory-motor representations by virtue of two properties: broad generality and tolerance to the absence of sensory-motor associations. We review three of our recent experiments that employ these criteria in order to localize neural representations of several specific kinds of nonsensory attributes: functions, intentions, and belief traits. Building on past work, we find that neuroimaging evidence can be used fruitfully to distinguish interesting hypotheses about neural organization. On the other hand, most such evidence does not speak to any clear notion of “grounding” or “embodiment,” because these terms do not make clear, specific, empirical predictions. We argue that cognitive neuroscience will proceed most fruitfully by relinquishing these terms.

Edigi, G., & Caramazza, A. (2016). Integration Processes Compared: Cortical Differences for Consistency Evaluation and Passive Comprehension in Local and Global Coherence. Journal of Cognitive Neuroscience.Abstract

This research studies the neural systems underlying two integration processes that take place during natural discourse comprehension: consistency evaluation and passive comprehension. Evaluation was operationalized with a consistency judgment task and passive comprehension with a passive listening task. Using fMRI, the experiment examined the integration of incoming sentences with more recent, local context and with more distal, global context in these two tasks. The stimuli were stories in which we manipulated the consistency of the endings with the local context and the relevance of the global context for the integration of the endings. A whole-brain analysis revealed several differences between the two tasks. Two networks previously associated with semantic processing and attention orienting showed more activation during the judgment than the passive listening task. A network previously associated with episodic memory retrieval and construction of mental scenes showed greater activity when global context was relevant, but only during the judgment task. This suggests that evaluation, more than passive listening, triggers the reinstantiation of global context and the construction of a rich mental model for the story. Finally, a network previously linked to fluent updating of a knowledge base showed greater activity for locally consistent endings than inconsistent ones, but only during passive listening, suggesting a mode of comprehension that relies on a local scope approach to language processing. Taken together, these results show that consistency evaluation and passive comprehension weigh differently on distal and local information and are implemented, in part, by different brain networks.

Vannuscorps, G., & Caramazza, A. (2016). The origin of the biomechanical bias in apparent body movement perception. Neuropsychologia.Abstract

The perception of apparent body movement sometimes follows biologically plausible paths rather than paths along the shortest distance as in the case for inanimate objects. For numerous authors, this demonstrates that the somatosensory and motor representations of the observer's own body support and constrain the perception of others’ body movements. In this paper, we report evidence that calls for a re-examination of this account. We presented an apparent upper limb movement perception task to typically developed participants and five individuals born without upper limbs who were, therefore, totally deprived of somatosensory or motor representations of those limbs. Like the typically developed participants, they showed the typical bias toward long and biomechanically plausible path. This finding suggests that the computations underlying the biomechanical bias in apparent body movement perception is intrinsic to the visual system.

Wang, X., Peelen, M. V., Han, Z., Caramazza, A., & Bi, Y. (2016). The role of vision in the neural representation of unique entities. Neuropsychologia , 87, 144-156. Full Text
Porter, K. B., Mazza, V., Garofalo, A., & Caramazza, A. (2016). Visual object individuation occurs over object wholes, parts, and even holes. Attention, Perception, & Psychophysics.Abstract

Segmentation of the world into meaningful units has typically been described as object individuation, emphasizing the spatially disconnected quality that comes as a result of objecthood. This segmentation can occur rapidly, even in parallel for multiple objects. It remains unclear whether objecthood is a necessary requirement for parallel individuation, or whether target features in distinct locations, such as object parts, may also be individuated in parallel. In a series of six experiments, we used a rapid enumeration task to test whether subitizing, a phenomenon believed to result from parallel individuation, occurs over object parts. We found that subitizing and individuation occur over connected object parts as well as physically separate objects of varied shapes and sizes. We also observed subitizing when target items are indents, features intrinsic to the shape of the object, and when cues for occlusion were removed. The results of these studies suggest that parallel individuation is not bound to objecthood, and can occur over object parts existing in separate locations.

Bi, Y., Wang, X., & Caramazza, A. (2016). Object Domain and Modality in the Ventral Visual Pathway. Trends in Cognitive Sciences , 20 (4), 282-290.Abstract

The nature of domain-specific organization in higher-order visual cortex (ventral occipital temporal cortex, VOTC) has been investigated both in the case of visual experience deprivation and of modality of stimulation in sighted individuals. Object domain interacts in an intriguing and revelatory way with visual experience and modality of stimulation: selectivity for artifacts and scene domains is largely immune to visual deprivation and is multi-modal, whereas selectivity for animate items in lateral posterior fusiform gyrus is present only with visual stimulation. This domain-by-modality interaction is not readily accommodated by existing theories of VOTC representation. We conjecture that these effects reflect a distinction between the visual features that characterize different object domains and their interaction with different types of downstream computational systems.

Vannuscorps, G., & Caramazza, A. (2016). Typical action perception and interpretation without motor simulation. Proceedings of the National Academy of Sciences , 113 (1), 86-91.Abstract

Every day, we interact with people synchronously, immediately understand what they are doing, and easily infer their mental state and the likely outcome of their actions from their kinematics. According to various motor simulation theories of perception, such efficient perceptual processing of othersactions cannot be achieved by visual analysis of the movements alone but requires a process of motor simulationan unconscious, covert imitation of the observed movements. According to this hypothesis, individ- uals incapable of simulating observed movements in their motor system should have difficulty perceiving and interpreting ob- served actions. Contrary to this prediction, we found across eight sensitive experiments that individuals born with absent or se- verely shortened upper limbs (upper limb dysplasia), despite some variability, could perceive, anticipate, predict, comprehend, and mem- orize upper limb actions, which they cannot simulate, as efficiently as typically developed participants. We also found that, like the typically developed participants, the dysplasic participants systematically per- ceived the position of moving upper limbs slightly ahead of their real position but only when the anticipated position was not biomechan- ically awkward. Such anticipatory bias and its modulation by implicit knowledge of the body biomechanical constraints were previously considered as indexes of the crucial role of motor simulation in action perception. Our findings undermine this assumption and the theories that place the locus of action perception and comprehension in the motor system and invite a shift in the focus of future research to the question of how the visuo-perceptual system represents and pro- cesses observed body movements and actions. 

Cheung, O., & Caramazza, A. (2015). Contextual influences on object representations in the occipito-temporal cortex. [Conference Abstract]. Journal of Vision , 15 (12), 1169.
Konkle, T., Wang, X., Peelen, M., Caramazza, A., & Bi, Y. (2015). Convergence and divergence in the neural organization of object responses to pictures and words. [Conference Abstract]. Journal of Vision , 15 (12), 375.
Anzellotti, S., & Caramazza, A. (2015). From Parts to Identity: Invariance and Sensitivity of Face Representations to Different Face Halves. Cerebral Cortex , 1-10. Full TextAbstract

Recognizing the identity of a face is computationally challenging, because it requires distinguishing between similar images depicting different people, while recognizing even very different images depicting a same person. Previous human fMRI studies investigated representations of face identity in the presence of changes in viewpoint and in expression. Despite the importance of holistic processing for face recognition, an investigation of representations of face identity across different face parts is missing. To fill this gap, we investigated representations of face identity and their invariance across different face halves. Information about face identity with invariance across changes in the face half was individuated in the right anterior temporal lobe, indicating this region as the most plausible candidate brain area for the representation of face identity. In a complementary analysis, information distinguishing between different face halves was found to decline along the posterior to anterior axis in the ventral stream.