Distinct Neural Components of Visually Guided Grasping during Planning and Execution.

Selecting suitable grasps on three-dimensional objects is a challenging visuomotor computation, which involves combining information about an object (e.g., its shape, size, and mass) with information about the actor's body (e.g., the optimal grasp aperture and hand posture for comfortable manipulation). Here, we used functional magnetic resonance imaging to investigate brain networks associated with these distinct aspects during grasp planning and execution. Human participants of either sex viewed and then executed preselected grasps on L-shaped objects made of wood and/or brass. By leveraging a computational approach that accurately predicts human grasp locations, we selected grasp points that disentangled the role of multiple grasp-relevant factors, that is, grasp axis, grasp size, and object mass. Representational Similarity Analysis revealed that grasp axis was encoded along dorsal-stream regions during grasp planning. Grasp size was first encoded in ventral stream areas during grasp planning then in premotor regions during grasp execution. Object mass was encoded in ventral stream and (pre)motor regions only during grasp execution. Premotor regions further encoded visual predictions of grasp comfort, whereas the ventral stream encoded grasp comfort during execution, suggesting its involvement in haptic evaluation. These shifts in neural representations thus capture the sensorimotor transformations that allow humans to grasp objects.SIGNIFICANCE STATEMENT Grasping requires integrating object properties with constraints on hand and arm postures. Using a computational approach that accurately predicts human grasp locations by combining such constraints, we selected grasps on objects that disentangled the relative contributions of object mass, grasp size, and grasp axis during grasp planning and execution in a neuroimaging study. Our findings reveal a greater role of dorsal-stream visuomotor areas during grasp planning, and, surprisingly, increasing ventral stream engagement during execution. We propose that during planning, visuomotor representations initially encode grasp axis and size. Perceptual representations of object material properties become more relevant instead as the hand approaches the object and motor programs are refined with estimates of the grip forces required to successfully lift the object.

The role of animal faces in the animate-inanimate distinction in the ventral temporal cortex.

Animate and inanimate objects elicit distinct response patterns in the human ventral temporal cortex (VTC), but the exact features driving this distinction are still poorly understood. One prominent feature that distinguishes typical animals from inanimate objects and that could potentially explain the animate-inanimate distinction in the VTC is the presence of a face. In the current fMRI study, we investigated this possibility by creating a stimulus set that included animals with faces, faceless animals, and inanimate objects, carefully matched in order to minimize other visual differences. We used both searchlight-based and ROI-based representational similarity analysis (RSA) to test whether the presence of a face explains the animate-inanimate distinction in the VTC. The searchlight analysis revealed that when animals with faces were removed from the analysis, the animate-inanimate distinction almost disappeared. The ROI-based RSA revealed a similar pattern of results, but also showed that, even in the absence of faces, information about agency (a combination of animal's ability to move and think) is present in parts of the VTC that are sensitive to animacy. Together, these analyses showed that animals with faces do elicit a stronger animate/inanimate response in the VTC, but that faces are not necessary in order to observe high-level animacy information (e.g., agency) in parts of the VTC. A possible explanation could be that this animacy-related activity is driven not by faces per se, or the visual features of faces, but by other factors that correlate with face presence, such as the capacity for self-movement and thought. In short, the VTC might treat the face as a proxy for agency, a ubiquitous feature of familiar animals.

Activity in perirhinal and entorhinal cortex predicts perceived visual similarities among category exemplars with highest precision.

Vision neuroscience has made great strides in understanding the hierarchical organization of object representations along the ventral visual stream (VVS). How VVS representations capture fine-grained visual similarities between objects that observers subjectively perceive has received limited examination so far. In the current study, we addressed this question by focussing on perceived visual similarities among subordinate exemplars of real-world categories. We hypothesized that these perceived similarities are reflected with highest fidelity in neural activity patterns downstream from inferotemporal regions, namely in perirhinal (PrC) and anterolateral entorhinal cortex (alErC) in the medial temporal lobe. To address this issue with functional magnetic resonance imaging (fMRI), we administered a modified 1-back task that required discrimination between category exemplars as well as categorization. Further, we obtained observer-specific ratings of perceived visual similarities, which predicted behavioural discrimination performance during scanning. As anticipated, we found that activity patterns in PrC and alErC predicted the structure of perceived visual similarity relationships among category exemplars, including its observer-specific component, with higher precision than any other VVS region. Our findings provide new evidence that subjective aspects of object perception that rely on fine-grained visual differentiation are reflected with highest fidelity in the medial temporal lobe.

The nature of the animacy organization in human ventral temporal cortex.

The principles underlying the animacy organization of the ventral temporal cortex (VTC) remain hotly debated, with recent evidence pointing to an animacy continuum rather than a dichotomy. What drives this continuum? According to the visual categorization hypothesis, the continuum reflects the degree to which animals contain animal-diagnostic features. By contrast, the agency hypothesis posits that the continuum reflects the degree to which animals are perceived as (social) agents. Here, we tested both hypotheses with a stimulus set in which visual categorizability and agency were dissociated based on representations in convolutional neural networks and behavioral experiments. Using fMRI, we found that visual categorizability and agency explained independent components of the animacy continuum in VTC. Modeled together, they fully explained the animacy continuum. Finally, clusters explained by visual categorizability were localized posterior to clusters explained by agency. These results show that multiple organizing principles, including agency, underlie the animacy continuum in VTC.

MEG sensor patterns reflect perceptual but not categorical similarity of animate and inanimate objects.

Human high-level visual cortex shows a distinction between animate and inanimate objects, as revealed by fMRI. Recent studies have shown that object animacy can similarly be decoded from MEG sensor patterns. Which object properties drive this decoding? Here, we disentangled the influence of perceptual and categorical object properties by presenting perceptually matched objects (e.g., snake and rope) that were nonetheless easily recognizable as being animate or inanimate. In a series of behavioral experiments, three aspects of perceptual dissimilarity of these objects were quantified: overall dissimilarity, outline dissimilarity, and texture dissimilarity. Neural dissimilarity of MEG sensor patterns was modeled using regression analysis, in which perceptual dissimilarity (from the behavioral experiments) and categorical dissimilarity served as predictors of neural dissimilarity. We found that perceptual dissimilarity was strongly reflected in MEG sensor patterns from 80 ms after stimulus onset, with separable contributions of outline and texture dissimilarity. Surprisingly, when controlling for perceptual dissimilarity, MEG patterns did not carry information about object category (animate vs inanimate) at any time point. Nearly identical results were found in a second MEG experiment that required basic-level object recognition. This is in contrast to results observed in fMRI using the same stimuli, task, and analysis approach: fMRI voxel patterns in object-selective cortex showed a highly reliable categorical distinction even when controlling for perceptual dissimilarity. These results suggest that MEG sensor patterns do not capture object animacy independently of perceptual differences between animate and inanimate objects.

Disentangling Representations of Object Shape and Object Category in Human Visual Cortex: The Animate-Inanimate Distinction.

Objects belonging to different categories evoke reliably different fMRI activity patterns in human occipitotemporal cortex, with the most prominent distinction being that between animate and inanimate objects. An unresolved question is whether these categorical distinctions reflect category-associated visual properties of objects or whether they genuinely reflect object category. Here, we addressed this question by measuring fMRI responses to animate and inanimate objects that were closely matched for shape and low-level visual features. Univariate contrasts revealed animate- and inanimate-preferring regions in ventral and lateral temporal cortex even for individually matched object pairs (e.g., snake-rope). Using representational similarity analysis, we mapped out brain regions in which the pairwise dissimilarity of multivoxel activity patterns (neural dissimilarity) was predicted by the objects' pairwise visual dissimilarity and/or their categorical dissimilarity. Visual dissimilarity was measured as the time it took participants to find a unique target among identical distractors in three visual search experiments, where we separately quantified overall dissimilarity, outline dissimilarity, and texture dissimilarity. All three visual dissimilarity structures predicted neural dissimilarity in regions of visual cortex. Interestingly, these analyses revealed several clusters in which categorical dissimilarity predicted neural dissimilarity after regressing out visual dissimilarity. Together, these results suggest that the animate-inanimate organization of human visual cortex is not fully explained by differences in the characteristic shape or texture properties of animals and inanimate objects. Instead, representations of visual object properties and object category may coexist in more anterior parts of the visual system.