Lateral Occipitotemporal Cortex Research Articles

A radial template space reveals organization of feature and task-selective regions in lateral occipitotemporal cortex

A radial template space reveals organization of feature and task-selective regions in lateral occipitotemporal cortex

Sensitivity and specificity of the action observation network to kinematics, target object, and gesture meaning.

Hierarchical models have been proposed to explain how the brain encodes actions, whereby different areas represent different features, such as gesture kinematics, target object, action goal, and meaning. The visual processing of action-related information is distributed over a well-known network of brain regions spanning separate anatomical areas, attuned to specific stimulus properties, and referred to as action observation network (AON). To determine the brain organization of these features, we measured representational geometries during the observation of a large set of transitive and intransitive gestures in two independent functional magnetic resonance imaging experiments. We provided evidence for a partial dissociation between kinematics, object characteristics, and action meaning in the occipito-parietal, ventro-temporal, and lateral occipito-temporal cortex, respectively. Importantly, most of the AON showed low specificity to all the explored features, and representational spaces sharing similar information content were spread across the cortex without being anatomically adjacent. Overall, our results support the notion that the AON relies on overlapping and distributed coding and may act as a unique representational space instead of mapping features in a modular and segregated manner.

Temporal dynamics of short-term neural adaptation across human visual cortex.

Neural responses in visual cortex adapt to prolonged and repeated stimuli. While adaptation occurs across the visual cortex, it is unclear how adaptation patterns and computational mechanisms differ across the visual hierarchy. Here we characterize two signatures of short-term neural adaptation in time-varying intracranial electroencephalography (iEEG) data collected while participants viewed naturalistic image categories varying in duration and repetition interval. Ventral- and lateral-occipitotemporal cortex exhibit slower and prolonged adaptation to single stimuli and slower recovery from adaptation to repeated stimuli compared to V1-V3. For category-selective electrodes, recovery from adaptation is slower for preferred than non-preferred stimuli. To model neural adaptation we augment our delayed divisive normalization (DN) model by scaling the input strength as a function of stimulus category, enabling the model to accurately predict neural responses across multiple image categories. The model fits suggest that differences in adaptation patterns arise from slower normalization dynamics in higher visual areas interacting with differences in input strength resulting from category selectivity. Our results reveal systematic differences in temporal adaptation of neural population responses between lower and higher visual brain areas and show that a single computational model of history-dependent normalization dynamics, fit with area-specific parameters, accounts for these differences.

Reciprocal interactions among parietal and occipito-temporal representations support everyday object-directed actions

Everyday interactions with common manipulable objects require the integration of conceptual knowledge about objects and actions with real-time sensory information about the position, orientation and volumetric structure of the grasp target. The ability to successfully interact with everyday objects involves analysis of visual form and shape, surface texture, material properties, conceptual attributes such as identity, function and typical context, and visuomotor processing supporting hand transport, grasp form, and object manipulation. Functionally separable brain regions across the dorsal and ventral visual pathways support the processing of these different object properties and, in cohort, are necessary for functional object use. Object-directed grasps display end-state-comfort: they anticipate in form and force the shape and material properties of the grasp target, and how the object will be manipulated after it is grasped. End-state-comfort is the default for everyday interactions with manipulable objects and implies integration of information across the ventral and dorsal visual pathways. We propose a model of how visuomotor and action representations in parietal cortex interact with object representations in ventral and lateral occipito-temporal cortex. One pathway, from the supramarginal gyrus to the middle and inferior temporal gyrus, supports the integration of action-related information, including hand and limb position (supramarginal gyrus) with conceptual attributes and an appreciation of the action goal (middle temporal gyrus). A second pathway, from posterior IPS to the fusiform gyrus and collateral sulcus supports the integration of grasp parameters (IPS) with the surface texture and material properties (e.g., weight distribution) of the grasp target. Reciprocal interactions among these regions are part of a broader network of regions that support everyday functional object interactions.

Overlapping representations of observed actions and action-related features.

The lateral occipitotemporal cortex (LOTC) has been shown to capture the representational structure of a smaller range of actions. In the current study, we carried out an fMRI experiment in which we presented human participants with images depicting 100 different actions and used representational similarity analysis (RSA) to determine which brain regions capture the semantic action space established using judgments of action similarity. Moreover, to determine the contribution of a wide range of action-related features to the neural representation of the semantic action space we constructed an action feature model on the basis of ratings of 44 different features. We found that the semantic action space model and the action feature model are best captured by overlapping activation patterns in bilateral LOTC and ventral occipitotemporal cortex (VOTC). An RSA on eight dimensions resulting from principal component analysis carried out on the action feature model revealed partly overlapping representations within bilateral LOTC, VOTC, and the parietal lobe. Our results suggest spatially overlapping representations of the semantic action space of a wide range of actions and the corresponding action-related features. Together, our results add to our understanding of the kind of representations along the LOTC that support action understanding.

Incidental visual processing of spatiotemporal cues in communicative interactions: An fMRI investigation

Abstract The interpretation of social interactions between people is important in many daily situations. The coordination of the relative body movements between them may provide visual cues that observers use without attention to discriminate such social interactions from the actions of people acting independently of each other. Previous studies highlighted brain regions involved in the visual processing of interacting versus independently acting people, including posterior superior temporal sulcus, and areas of lateral occipitotemporal and parietal cortices. Unlike these previous studies, we focused on the incidental visual processing of social interactions; that is, the processing of the body movements outside the observers’ focus of attention. In the current study, we used functional imaging to measure brain activation while participants were presented with point-light dyads portraying communicative interactions or individual actions. However, their task was to discriminate the brightness of two crosses also on the screen. To investigate brain regions that may process the spatial and temporal relationships between the point-light displays, we either reversed the facing direction of one agent or spatially scrambled the local motion of the points. Incidental processing of communicative interactions elicited activation in right anterior STS only when the two agents were facing each other. Controlling for differences in local motion by subtracting brain activation to scrambled versions of the point-light displays revealed significant activation in parietal cortex for communicative interactions, as well as left amygdala and brain stem/cerebellum. Our results complement previous studies and suggest that additional brain regions may be recruited to incidentally process the spatial and temporal contingencies that distinguish people acting together from people acting individually.

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 an fMRI-based multivariate pattern analysis (MVPA), 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. A total of 29 human participants (nine male) participated in the study. 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 a 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.

Minor Changes Change Memories: Functional Magnetic Resonance Imaging and Behavioral Reflections of Episodic Prediction Errors.

Episodic memories can be modified, a process that is potentially driven by mnemonic prediction errors. In the present study, we used modified cues to induce prediction errors of different episodic relevance. Participants encoded episodes in the form of short toy stories and then returned for an fMRI session on the subsequent day. Here, participants were presented either original episodes or slightly modified versions thereof. Modifications consisted of replacing a single object within the episode and either challenged the gist of an episode (gist modifications) or left it intact (surface modifications). On the next day, participants completed a post-fMRI memory test that probed memories for originally encoded episodes. Both types of modifications triggered brain activation in regions we previously found to be involved in the processing of content-based mnemonic prediction errors (i.e., the exchange of an object). Specifically, these were ventrolateral pFC, intraparietal cortex, and lateral occipitotemporal cortex. In addition, gist modifications triggered pronounced brain responses, whereas those for surface modification were only significant in the right inferior frontal sulcus. Processing of gist modifications also involved the posterior temporal cortex and the precuneus. Interestingly, our findings confirmed the posterior hippocampal role of detail processing in episodic memory, as evidenced by increased posterior hippocampal activity for surface modifications compared with gist modifications. In the post-fMRI memory test, previous experience with surface modified, but not gist-modified episodes, increased erroneous acceptance of the same modified versions as originally encoded. Whereas surface-level prediction errors might increase uncertainty and facilitate confusion of alternative episode representations, gist-level prediction errors seem to trigger the clear distinction of independent episodes.

The Representation of Observed Actions at the Subordinate, Basic, and Superordinate Level.

Actions can be planned and recognized at different hierarchical levels, ranging from very specific (e.g., to swim backstroke) to very broad (e.g., locomotion). Understanding the corresponding neural representation is an important prerequisite to reveal how our brain flexibly assigns meaning to the world around us. To address this question, we conducted an event-related fMRI study in male and female human participants in which we examined distinct representations of observed actions at the subordinate, basic and superordinate level. Using multiple regression representational similarity analysis (RSA) in predefined regions of interest, we found that the three different taxonomic levels were best captured by patterns of activations in bilateral lateral occipitotemporal cortex (LOTC), showing the highest similarity with the basic level model. A whole-brain multiple regression RSA revealed that information unique to the basic level was captured by patterns of activation in dorsal and ventral portions of the LOTC and in parietal regions. By contrast, the unique information for the subordinate level was limited to bilateral occipitotemporal cortex, while no single cluster was obtained that captured unique information for the superordinate level. The behaviorally established action space was best captured by patterns of activation in the LOTC and superior parietal cortex, and the corresponding neural patterns of activation showed the highest similarity with patterns of activation corresponding to the basic level model. Together, our results suggest that occipitotemporal cortex shows a preference for the basic level model, with flexible access across the subordinate and the basic level.SIGNIFICANCE STATEMENT The human brain captures information at varying levels of abstraction. It is debated which brain regions host representations across different hierarchical levels, with some studies emphasizing parietal and premotor regions, while other studies highlight the role of the lateral occipitotemporal cortex (LOTC). To shed light on this debate, here we examined the representation of observed actions at the three taxonomic levels suggested by Rosch et al. (1976) Our results highlight the role of the LOTC, which hosts a shared representation across the subordinate and the basic level, with the highest similarity with the basic level model. These results shed new light on the hierarchical organization of observed actions and provide insights into the neural basis underlying the basic level advantage.

Where in the brain do internally generated and externally presented visual information interact?

Conscious experiences normally result from the flow of external input into our sensory systems. However, we can also create conscious percepts independently of sensory stimulation. These internally generated percepts are referred to as mental images, and they have many similarities with real visual percepts. Consequently, mental imagery is often referred to as “seeing in the mind’s eye”. While the neural basis of imagery has been widely studied, the interaction between internal and external sources of visual information has received little interest. Here we examined this question by using fMRI to record brain activity of healthy human volunteers while they were performing visual imagery that was distracted with a concurrent presentation of a visual stimulus. Multivariate pattern analysis (MVPA) was used to identify the brain basis of this interaction. Visual imagery was reflected in several brain areas in ventral temporal, lateral occipitotemporal, and posterior frontal cortices, with a left-hemisphere dominance. The key finding was that imagery content representations in the left lateral occipitotemporal cortex were disrupted when a visual distractor was presented during imagery. Our results thus demonstrate that the representations of internal and external visual information interact in brain areas associated with the encoding of visual objects and shapes.

Contralateral Biases in Category-selective Areas Are Stronger in the Left Hemisphere than the Right Hemisphere.

Contralateral bias is a well-known feature of early visual cortex, but how it varies across higher-level, category-selective visual cortex and how much that bias differs between preferred and nonpreferred is unclear. Here, we examined 12 category-selective regions across 4 experiments using peripherally presented faces, bodies, houses, and scenes, to measure the difference in contralateral bias between preferred and nonpreferred stimuli. The results showed a substantial range of contralateral biases across the category-selective regions, similar to prior studies using category-selective stimuli [Silson, E. H., Groen, I. I., & Baker, C. I. Direct comparison of contralateral bias and face/scene selectivity in human occipitotemporal cortex. Brain Structure and Function, 227, 1405-1421, 2022; Gomez, J., Natu, V., Jeska, B., Barnett, M., & Grill-Spector, K. Development differentially sculpts receptive fields across early and high-level human visual cortex. Nature Communications, 9, 788, 2018; Silson, E. H., Groen, I. I. A., Kravitz, D. J., & Baker, C. I. Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex. Journal of Vision, 16, 14, 2016; Kay, K. N., Weiner, K. S., & Grill-Spector, K. Attention reduces spatial uncertainty in human ventral temporal cortex. Current Biology, 25, 595-600, 2015; Silson, E. H., Chan, A. W.-Y., Reynolds, R. C., Kravitz, D. J., & Baker, C. I. A retinotopic basis for the division of high-level scene processing between lateral and ventral human occipitotemporal cortex. Journal of Neuroscience, 35, 11921-11935, 2015]. These contralateral biases were stronger in the left hemisphere regions than right, an asymmetry that was unchanged even when participants performed an attentionally demanding task. Thus, corresponding pairs of category-selective regions (e.g., left fusiform face area [lFFA] and right FFA [rFFA]) do not appear to be mirror images of each other; instead, the right hemisphere regions engage in greater integration of information from the two hemifields. The rFFA and right fusiform body area-both located on the right lateral fusiform gyrus-consistently had the weakest contralateral biases. That this asymmetry was most pronounced in the fusiform gyrus may account for why a unilateral lesion to the rFFA but not the lFFA can produce prosopagnosia. Together, our findings demonstrate that category-selective areas show pronounced differences in the extent of their contralateral biases and that a consistent asymmetry in the strength of the contralateral biases exists between the two hemispheres.

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.

Functional relevance of the extrastriate body area for visual and haptic object recognition: a preregistered fMRI-guided TMS study.

The extrastriate body area (EBA) is a region in the lateral occipito-temporal cortex (LOTC), which is sensitive to perceived body parts. Neuroimaging studies suggested that EBA is related to body and tool processing, regardless of the sensory modalities. However, how essential this region is for visual tool processing and nonvisual object processing remains a matter of controversy. In this preregistered fMRI-guided repetitive transcranial magnetic stimulation (rTMS) study, we examined the causal involvement of EBA in multisensory body and tool recognition. Participants used either vision or haptics to identify 3 object categories: hands, teapots (tools), and cars (control objects). Continuous theta-burst stimulation (cTBS) was applied over left EBA, right EBA, or vertex (control site). Performance for visually perceived hands and teapots (relative to cars) was more strongly disrupted by cTBS over left EBA than over the vertex, whereas no such object-specific effect was observed in haptics. The simulation of the induced electric fields confirmed that the cTBS affected regions including EBA. These results indicate that the LOTC is functionally relevant for visual hand and tool processing, whereas the rTMS over EBA may differently affect object recognition between the 2 sensory modalities.

Face pareidolia is enhanced by 40 Hz transcranial alternating current stimulation (tACS) of the face perception network

Pareidolia refers to the perception of ambiguous sensory patterns as carrying a specific meaning. In its most common form, pareidolia involves human-like facial features, where random objects or patterns are illusionary recognized as faces. The current study investigated the neurophysiological correlates of face pareidolia via transcranial alternating current stimulation (tACS). tACS was delivered at gamma (40 Hz) frequency over critical nodes of the “face perception” network (i.e., right lateral occipito-temporal and left prefrontal cortex) of 75 healthy participants while completing four face perception tasks (‘Mooney test’ for faces, ‘Toast test’, ‘Noise pareidolia test’, ‘Pareidolia task’) and an object perception task (‘Mooney test’ for objects). In this single-blind, sham-controlled between-subjects study, participants received 35 min of either Sham, Online, (40Hz-tACS_ON), or Offline (40Hz-tACS_PRE) stimulation. Results showed that face pareidolia was causally enhanced by 40Hz-tACS_PRE in the Mooney test for faces in which, as compared to sham, participants more often misperceived scrambled stimuli as faces. In addition, as compared to sham, participants receiving 40Hz-tACS_PRE showed similar reaction times (RTs) when perceiving illusory faces and correctly recognizing noise stimuli in the Toast test, thus not exhibiting hesitancy in identifying faces where there were none. Also, 40Hz-tACS_ON induced slower rejections of face pareidolia responses in the Noise pareidolia test. The current study indicates that 40 Hz tACS can enhance pareidolic illusions in healthy individuals and, thus, that high frequency (i.e., gamma band) oscillations are critical in forming coherent and meaningful visual perception.

Involvement of the posterior tool processing network during explicit retrieval of action tool and semantic tool knowledge: an fMRI study.

Our ability to understand how to interact with familiar objects is supported by conceptual tool knowledge. Conceptual tool knowledge includes action tool and semantic tool knowledge which are supported by the ventro-dorsal and the ventral pathways, respectively. This apparent functional segregation has been recently called into question. In a block-design fMRI study, 35 participants were asked to complete manipulation, function, and association judgment tasks about pairs of familiar objects. Our results showed that lateral occipitotemporal cortex in the ventral pathway was more sensitive to manipulation and function judgment tasks compared with association judgment tasks. Functional connectivity analyses revealed distinct coupling patterns between inferior parietal lobule, lateral occipitotemporal cortex, and fusiform gyrus. Taken together, these data indicate that action tool and semantic tool knowledge are both supported by ventral and ventro-dorsal pathways. Moreover, the explicit retrieval of these representations is supported by the functional coupling of common and distinct brain regions of the posterior tool processing network varying according to the kind of relations to be retrieved.

Novel objects with causal event schemas elicit selective responses in tool- and hand-selective lateral occipitotemporal cortex.

Tool-selective lateral occipitotemporal cortex (LOTC) responds preferentially to images of tools (hammers, brushes) relative to non-tool objects (clocks, shoes). What drives these responses? Unlike other objects, tools exert effects on their surroundings. We tested whether LOTC responses are influenced by event schemas that denote different temporal relations. Participants learned about novel objects embedded in different event sequences. Causer objects moved prior to the appearance of an environmental event (e.g. stars), while Reactor objects moved after an event. Visual features and motor association were controlled. During functional magnetic resonance imaging, participants viewed still images of the objects. We localized tool-selective LOTC and non-tool-selective parahippocampal cortex (PHC) by contrasting neural responses to images of familiar tools and non-tools. We found that LOTC responded more to Causers than Reactors, while PHC did not. We also measured responses to images of hands, which elicit overlapping responses with tools. Across inferior temporal cortex, voxels' tool and hand selectivity positively predicted a preferential response to Causers. We conclude that an event schema typical of tools is sufficient to drive LOTC and that category-preferential responses across the temporal lobe may reflect relational event structures typical of those domains.

When action prediction grows old: An fMRI study.

Predicting the unfolding of others' actions (action prediction) is crucial for successfully navigating the social world and interacting efficiently. Age-related changes in this domain have remained largely unexplored, especially for predictions regarding simple gestures and independent of contextual information or motor expertise. Here, we evaluated whether healthy aging impacts the neurophysiological processes recruited to anticipate, from the observation of implied-motion postures, the correct conclusion of simple grasping and pointing actions. A color-discrimination task served as a control condition to assess the specificity of the age-related effects. Older adults showed reduced efficiency in performance that was yet not specific to the action prediction task. Nevertheless, fMRI results revealed task-specific age-related differences: while both groups showed stronger recruitment of the lateral occipito-temporal cortex bilaterally during the action prediction than the control task, the younger participants additionally showed a higher bilateral engagement of parietal regions. Importantly, in both groups, the recruitment of visuo-motor processes in the right posterior parietal cortex was a predictor of good performance. These results support the hypothesis of decreased involvement of sensorimotor processes in cognitive tasks when processing action- and body-related stimuli in healthy aging. These results have implications for social interaction, which requires the fast reading of others' gestures.

Efficient and effective assessment of deficits and their neural bases in stroke aphasia

ObjectiveMulti-assessment batteries are necessary for diagnosing and quantifying the multifaceted deficits observed post-stroke. Extensive batteries are thorough but impractically long for clinical settings or large-scale research studies. Clinically-targeted “shallow” batteries superficially cover a wide range of language skills relatively quickly but can struggle to identify mild deficits or quantify the impairment level. Our aim was to compare these batteries across a large group of chronic stroke aphasia and to test a novel data-driven reduced version of an extensive battery that maintained sensitivity to mild impairment, ability to grade deficits and the underlying component structure. MethodsWe tested 75 chronic left-sided stroke participants, spanning global to mild aphasia. The underlying structure of these three batteries was analysed using cross-validation and principal component analysis, in addition to univariate and multivariate lesion-symptom mapping. ResultsThis revealed a four-factor solution for the extensive and data-reduced batteries, identifying phonology, semantic skills, fluency and executive function in contrast to a two-factor solution using the shallow battery (language severity and cognitive severity). Lesion symptom mapping using participants’ factor scores identified convergent neural structures for phonology (superior temporal gyrus), semantics (inferior temporal gyrus), speech fluency (precentral gyrus) and executive function (lateral occipitotemporal cortex). The two shallow battery components converged with the phonology and executive function clusters. In addition, we show that multivariate models could predict the component scores using neural data, however not for every component. ConclusionsOverall, the data-driven battery appears to be an effective way to save time yet retain maintained sensitivity to mild impairment, ability to grade deficits and the underlying component structure observed in post-stroke aphasia.

Representation of motion concepts in occipitotemporal cortex: fMRI activation, decoding and connectivity analyses

Embodied theories of semantic cognition predict that brain regions involved in motion perception are engaged when people comprehend motion concepts expressed in language. Left lateral occipitotemporal cortex (LOTC) is implicated in both motion perception and motion concept processing but prior studies have produced mixed findings on which parts of this region are engaged by motion language. We scanned participants performing semantic judgements about sentences describing motion events and static events. We performed univariate analyses, multivariate pattern analyses (MVPA) and psychophysiological interaction (PPI) analyses to investigate the effect of motion on activity and connectivity in different parts of LOTC. In multivariate analyses that decoded whether a sentence described motion or not, the middle and posterior parts of LOTC showed above-chance level performance, with performance exceeding that of other brain regions. Univariate ROI analyses found the middle part of LOTC was more active for motion events than static ones. Finally, PPI analyses found that when processing motion events, the middle and posterior parts of LOTC (overlapping with motion perception regions), increased their connectivity with cognitive control regions. Taken together, these results indicate that the more posterior parts of LOTC, including motion perception cortex, respond differently to motion vs. static events. These findings are consistent with embodiment accounts of semantic processing, and suggest that understanding verbal descriptions of motion engages areas of the occipitotemporal cortex involved in perceiving motion.

Two distinct networks containing position-tolerant representations of actions in the human brain.

Humans can recognize others' actions in the social environment. This action recognition ability is rarely hindered by the movement of people in the environment. The neural basis of this position tolerance for observed actions is not fully understood. Here, we aimed to identify brain regions capable of generalizing representations of actions across different positions and investigate the representational content of these regions. In a functional magnetic resonance imaging experiment, participants viewed point-light displays of different human actions. Stimuli were presented in either the upper or the lower visual field. Multivariate pattern analysis and a surface-based searchlight approach were employed to identify brain regions that contain position-tolerant action representation: Classifiers were trained with patterns in response to stimuli presented in one position and were tested with stimuli presented in another position. Results showed above-chance classification in the left and right lateral occipitotemporal cortices, right intraparietal sulcus, and right postcentral gyrus. Further analyses exploring the representational content of these regions showed that responses in the lateral occipitotemporal regions were more related to subjective judgments, while those in the parietal regions were more related to objective measures. These results provide evidence for two networks that contain abstract representations of human actions with distinct representational content.