Prediction error processing and sharpening of expected information across the face-processing hierarchy.

The perception and neural processing of sensory information are strongly influenced by prior expectations. The integration of prior and sensory information can manifest through distinct underlying mechanisms: focusing on unexpected input, denoted as prediction error (PE) processing, or amplifying anticipated information via sharpened representation. In this study, we employed computational modeling using deep neural networks combined with representational similarity analyses of fMRI data to investigate these two processes during face perception. Participants were cued to see face images, some generated by morphing two faces, leading to ambiguity in face identity. We show that expected faces were identified faster and perception of ambiguous faces was shifted towards priors. Multivariate analyses uncovered evidence for PE processing across and beyond the face-processing hierarchy from the occipital face area (OFA), via the fusiform face area, to the anterior temporal lobe, and suggest sharpened representations in the OFA. Our findings support the proposition that the brain represents faces grounded in prior expectations.

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.

Moving in response to an unseen visual stimulus.

OBJECTIVE: Whether consciousness has a causal role in voluntary movements is not clear. Backward masking blocks a stimulus from becoming conscious, but it can trigger movement in a reaction time paradigm. We hypothesize that if backward masking is used in a choice reaction time paradigm, when the visible stimulus (S2) differs from the masked stimulus (S1), the movement will often differ from conscious intent. We did such a study employing electroencephalography (EEG) to explore the brain activity associated with this effect. METHODS: Twenty healthy adults participated in a choice reaction time task with a backwardly masked stimulus and EEG. They moved right or left hand in response to the direction of an arrow. S2 was congruent or incongruent with S1. When incongruent, responses were frequently concordant with S1, with faster reaction time than when responding to S2 and thought to be a mistake. RESULTS: We show that it is possible to trigger movements from the unperceived stimuli indicating consciousness is not causal since the movement was not in accord with intent. EEG showed information flow from occipital cortex to motor cortex. CONCLUSIONS: Occipital activity was the same despite response, but the parietal and frontal EEG differed. When responding to S1, the motor cortex responded as soon as information arrived, and when responding to S2, the motor cortex responded with a delay allowing for other brain processing prior to movement initiation. While the exact time of conscious recognition of S2 is not clear, when there is a response to S1, the frontal cortex signals an "error", but this is apparently too late to veto the movement. SIGNIFICANCE: While consciousness does not initiate the movement, it monitors the concordance of intent and result.

Ventral and dorsal aspects of the inferior frontal-occipital fasciculus support verbal semantic access and visually-guided behavioural control.

The Inferior Frontal Occipital Fasciculus (IFOF) is a major anterior-to-posterior white matter pathway in the ventral human brain that connects parietal, temporal and occipital regions to frontal cortex. It has been implicated in a range of functions, including language, semantics, inhibition and the control of action. The recent research shows that the IFOF can be sub-divided into a ventral and dorsal branch, but the functional relevance of this distinction, as well as any potential hemispheric differences, are poorly understood. Using DTI tractography, we investigated the involvement of dorsal and ventral subdivisions of the IFOF in the left and right hemisphere in a response inhibition task (Go/No-Go), where the decision to respond or to withhold a prepotent response was made on the basis of semantic or non-semantic aspects of visual inputs. The task also varied the presentation modality (whether concepts were presented as written words or images). The results showed that the integrity of both dorsal and ventral IFOF in the left hemisphere were associated with participants' inhibition performance when the signal to stop was meaningful and presented in the verbal modality. This effect was absent in the right hemisphere. The integrity of dorsal IFOF was also associated with participants' inhibition efficiency in difficult perceptually guided decisions. This pattern of results indicates that left dorsal IFOF is implicated in the domain-general control of visually-guided behaviour, while the left ventral branch might interface with the semantic system to support the control of action when the inhibitory signal is based on meaning.

The development of orthography and phonology coupling in the ventral occipito-temporal cortex and its relation to reading.

The left ventral occipito-temporal (lvOT) cortex is considered to house the brain's representation of orthography (i.e., the spelling patterns of words). Because letter-sound coupling is crucial in reading, we investigated the engagement of the lvOT cortex in processing phonology (i.e., the sound patterns of words) as a function of reading acquisition. We tested 47 Polish children both at the beginning of formal literacy instruction and 2 years later. During functional magnetic resonance imaging, children performed auditory phonological tasks from small to large grain size levels (i.e., single phoneme, rhyme). We showed that orthographically relevant lvOT areas activated during small-grain size phonological tasks were skill-dependent, perhaps due to the relatively transparent mappings between orthography and phonology in Polish. We also studied activation pattern similarity between processing visual and auditory word stimuli in the lvOT. We found that a higher similarity level was observed in the anterior lvOT compared to the posterior lvOT after 2 years of schooling. This is consistent with models proposing a posterior-to-anterior shift in word processing during reading acquisition. We argue that the development of orthography-phonology coupling at the brain level reflects writing system-specific effects and a more universal pathway of the left vOT development in reading acquisition. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Neural basis of social attention: common and distinct mechanisms for social and nonsocial orienting stimuli.

Social and nonsocial directional stimuli (such as gaze and arrows, respectively) share their ability to trigger attentional processes, although the issue of whether social stimuli generate other additional (and unique) attentional effects is still under debate. In this study, we used the spatial interference paradigm to explore, using functional magnetic resonance imaging, shared and dissociable brain activations produced by gaze and arrows. Results showed a common set of regions (right parieto-temporo-occipital) similarly involved in conflict resolution for gaze and arrows stimuli, which showed stronger co-activation for incongruent than congruent trials. The frontal eye field showed stronger functional connectivity with occipital regions for congruent as compared with incongruent trials, and this effect was enhanced for gaze as compared with arrow stimuli in the right hemisphere. Moreover, spatial interference produced by incongruent (as compared with congruent) arrows was associated with increased functional coupling between the right frontal eye field and a set of regions in the left hemisphere. This result was not observed for incongruent (as compared with congruent) gaze stimuli. The right frontal eye field also showed greater coupling with left temporo-occipital regions for those conditions in which larger conflict was observed (arrow incongruent vs. gaze incongruent trials, and gaze congruent vs. arrow congruent trials). These findings support the view that social and nonsocial stimuli share some attentional mechanisms, while at the same time highlighting other differential effects. Highlights Attentional orienting triggered by social (gaze) and nonsocial (arrow) cues is comparable. When social and nonsocial stimuli are used as targets, qualitatively different behavioral effects are observed. This study explores the neural bases of shared and dissociable neural mechanisms for social and nonsocial stimuli. Shared mechanisms were found in the functional coupling between right parieto-temporo-occipital regions. Dissociable mechanisms were found in the functional coupling between right frontal eye field and ipsilateral and contralateral occipito-temporal regions.

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.

A "Bandwidth" in cortical representations of multiple faces.

The human ability to process multiple items simultaneously can be constrained by the extent to which those items are represented by distinct neural populations. In the current study, we used fMRI to investigate the cortical representation of multiple faces. We found that the addition of a second face to occupy both visual hemifields led to an increased response, whereas a further addition of faces within the same visual hemifield resulted in a decreased response. This pattern was widely observed in the occipital visual cortex, the intraparietal sulcus, and extended to the posterior inferotemporal cortex. A parallel trend was found in a behavioral change-detection task, revealing a perceptual "bandwidth" of multiface processing. The sensitivity to face clutter gradually decreased along the ventral pathway, supporting the notion of a buildup of clutter-tolerance representation. These cortical response patterns to face clutters suggest that adding signals with nonoverlapping cortical representation enhanced perception, while adding signals that competed for representation resources impaired perception.

Pontine Waves Accompanied by Short Hippocampal Sharp Wave-Ripples During Non-rapid Eye Movement Sleep.

Ponto-geniculo-occipital or pontine (P) waves have long been recognized as an electrophysiological signature of rapid eye movement (REM) sleep. However, P-waves can be observed not just during REM sleep, but also during non-REM (NREM) sleep. Recent studies have uncovered that P-waves are functionally coupled with hippocampal sharp wave ripples (SWRs) during NREM sleep. However, it remains unclear to what extent P-waves during NREM sleep share their characteristics with P-waves during REM sleep and how the functional coupling to P-waves modulates SWRs. Here, we address these issues by performing multiple types of electrophysiological recordings and fiber photometry in both sexes of mice. P-waves during NREM sleep share their waveform shapes and local neural ensemble dynamics at a short (~100 milliseconds) timescale with their REM sleep counterparts. However, the dynamics of mesopontine cholinergic neurons are distinct at a longer (~10 seconds) timescale: although P-waves are accompanied by cholinergic transients, the cholinergic tone gradually reduces before P-wave genesis during NREM sleep. While P-waves are coupled to hippocampal theta rhythms during REM sleep, P-waves during NREM sleep are accompanied by a rapid reduction in hippocampal ripple power. SWRs coupled with P-waves are short-lived and hippocampal neural firing is also reduced after P-waves. These results demonstrate that P-waves are part of coordinated sleep-related activity by functionally coupling with hippocampal ensembles in a state-dependent manner.

The effect of context congruency on fMRI repetition suppression for objects.

The recognition of objects is strongly facilitated when they are presented in the context of other objects (Biederman, 1972). Such contexts facilitate perception and induce expectations of context-congruent objects (Trapp and Bar, 2015). The neural mechanisms underlying these facilitatory effects of context on object processing, however, are not yet fully understood. In the present study, we investigate how context-induced expectations affect subsequent object processing. We used functional magnetic resonance imaging and measured repetition suppression as a proxy for prediction error processing. Participants viewed pairs of alternating or repeated object images which were preceded by context-congruent, context-incongruent or neutral cues. We found a stronger repetition suppression in congruent as compared to incongruent or neutral cues in the object sensitive lateral occipital cortex. Interestingly, this stronger effect was driven by enhanced responses to alternating stimulus pairs in the congruent contexts, rather than by suppressed responses to repeated stimulus pairs, which emphasizes the contribution of surprise-related response enhancement for the context modulation on RS when expectations are violated. In addition, in the congruent condition, we discovered significant functional connectivity between object-responsive and frontal cortical regions, as well as between object-responsive regions and the fusiform gyrus. Our findings indicate that prediction errors, reflected in enhanced brain responses to violated contextual expectations, underlie the facilitating effect of context during object perception.

Preferential signal pathways during the perception and imagery of familiar scenes: An effective connectivity study.

The perception and imagery of landmarks activate similar content-dependent brain areas, including occipital and temporo-medial brain regions. However, how these areas interact during visual perception and imagery of scenes, especially when recollecting their spatial location, remains unknown. Here, we combined functional magnetic resonance imaging (fMRI), resting-state functional connectivity (rs-fc), and effective connectivity to assess spontaneous fluctuations and task-induced modulation of signals among regions entailing scene-processing, the primary visual area and the hippocampus (HC), responsible for the retrieval of stored information. First, we functionally defined the scene-selective regions, that is, the occipital place area (OPA), the retrosplenial complex (RSC) and the parahippocampal place area (PPA), by using the face/scene localizer, observing that two portions of the PPA-anterior and posterior PPA-were consistently activated in all subjects. Second, the rs-fc analysis (n = 77) revealed a connectivity pathway similar to the one described in macaques, showing separate connectivity routes linking the anterior PPA with RSC and HC, and the posterior PPA with OPA. Third, we used dynamic causal modelling to evaluate whether the dynamic couplings among these regions differ between perception and imagery of familiar landmarks during a fMRI task (n = 16). We found a positive effect of HC on RSC during the retrieval of imagined places and an effect of occipital regions on both RSC and pPPA during the perception of scenes. Overall, we propose that under similar functional architecture at rest, different neural interactions take place between regions in the occipito-temporal higher-level visual cortex and the HC, subserving scene perception and imagery.

Humans predict the forest, not the trees: statistical learning of spatiotemporal structure in visual scenes.

The human brain is capable of using statistical regularities to predict future inputs. In the real world, such inputs typically comprise a collection of objects (e.g. a forest constitutes numerous trees). The present study aimed to investigate whether perceptual anticipation relies on lower-level or higher-level information. Specifically, we examined whether the human brain anticipates each object in a scene individually or anticipates the scene as a whole. To explore this issue, we first trained participants to associate co-occurring objects within fixed spatial arrangements. Meanwhile, participants implicitly learned temporal regularities between these displays. We then tested how spatial and temporal violations of the structure modulated behavior and neural activity in the visual system using fMRI. We found that participants only showed a behavioral advantage of temporal regularities when the displays conformed to their previously learned spatial structure, demonstrating that humans form configuration-specific temporal expectations instead of predicting individual objects. Similarly, we found suppression of neural responses for temporally expected compared with temporally unexpected objects in lateral occipital cortex only when the objects were embedded within expected configurations. Overall, our findings indicate that humans form expectations about object configurations, demonstrating the prioritization of higher-level over lower-level information in temporal expectation.

Patterns of multiple brain network activation in dot perspective task.

In this functional MRI (fMRI) study on 82 healthy adults using the dot perspective task, inconsistency of perspectives was associated with a significant increase of the mean reaction time and number of errors both in Self and Other conditions. Unlike the Arrow (non-mentalizing), the Avatar (mentalizing) paradigm was characterized by the recruitment of parts of the mentalizing and salience networks. These data provide experimental evidence supporting the fMRI distinction between mentalizing and non-mentalizing stimuli. A widespread activation of classical theory of mind (ToM) areas but also of salience network and decision making areas was observed in the Other compared to Self-conditions. Compared to Self-Consistent, Self-Inconsistent trials were related to increased activation in the lateral occipital cortex, right supramarginal and angular gyrus as well as inferior, superior and middle frontal gyri. Compared to the Other-Consistent, Other-Inconsistent trials yielded strong activation in the lateral occipital cortex, precuneus and superior parietal lobule, middle and superior precentral gyri and left frontal pole. These findings reveal that altercentric interference relies on areas involved in self-other distinction, self-updating and central executive functions. In contrast, egocentric interference needs the activation of the mirror neuron system and deductive reasoning, much less related to pure ToM abilities.

Angular Gyrus Responses Show Joint Statistical Dependence with Brain Regions Selective for Different Categories.

Category selectivity is a fundamental principle of organization of perceptual brain regions. Human occipitotemporal cortex is subdivided into areas that respond preferentially to faces, bodies, artifacts, and scenes. However, observers need to combine information about objects from different categories to form a coherent understanding of the world. How is this multicategory information encoded in the brain? Studying the multivariate interactions between brain regions of male and female human subjects with fMRI and artificial neural networks, we found that the angular gyrus shows joint statistical dependence with multiple category-selective regions. Adjacent regions show effects for the combination of scenes and each other category, suggesting that scenes provide a context to combine information about the world. Additional analyses revealed a cortical map of areas that encode information across different subsets of categories, indicating that multicategory information is not encoded in a single centralized location, but in multiple distinct brain regions.SIGNIFICANCE STATEMENT Many cognitive tasks require combining information about entities from different categories. However, visual information about different categorical objects is processed by separate, specialized brain regions. How is the joint representation from multiple category-selective regions implemented in the brain? Using fMRI movie data and state-of-the-art multivariate statistical dependence based on artificial neural networks, we identified the angular gyrus encoding responses across face-, body-, artifact-, and scene-selective regions. Further, we showed a cortical map of areas that encode information across different subsets of categories. These findings suggest that multicategory information is not encoded in a single centralized location, but at multiple cortical sites which might contribute to distinct cognitive functions, offering insights to understand integration in a variety of domains.

Distinct roles of forward and backward alpha-band waves in spatial visual attention.

Previous research has associated alpha-band [8-12 Hz] oscillations with inhibitory functions: for instance, several studies showed that visual attention increases alpha-band power in the hemisphere ipsilateral to the attended location. However, other studies demonstrated that alpha oscillations positively correlate with visual perception, hinting at different processes underlying their dynamics. Here, using an approach based on traveling waves, we demonstrate that there are two functionally distinct alpha-band oscillations propagating in different directions. We analyzed EEG recordings from three datasets of human participants performing a covert visual attention task (one new dataset with N = 16, two previously published datasets with N = 16 and N = 31). Participants were instructed to detect a brief target by covertly attending to the screen's left or right side. Our analysis reveals two distinct processes: allocating attention to one hemifield increases top-down alpha-band waves propagating from frontal to occipital regions ipsilateral to the attended location, both with and without visual stimulation. These top-down oscillatory waves correlate positively with alpha-band power in frontal and occipital regions. Yet, different alpha-band waves propagate from occipital to frontal regions and contralateral to the attended location. Crucially, these forward waves were present only during visual stimulation, suggesting a separate mechanism related to visual processing. Together, these results reveal two distinct processes reflected by different propagation directions, demonstrating the importance of considering oscillations as traveling waves when characterizing their functional role.

The occipital place area represents visual information about walking, not crawling.

Recent work has shown that the occipital place area (OPA)-a scene-selective region in adult humans-supports "visually guided navigation" (i.e. moving about the local visual environment and avoiding boundaries/obstacles). But what is the precise role of OPA in visually guided navigation? Considering humans move about their local environments beginning with crawling followed by walking, 1 possibility is that OPA is involved in both modes of locomotion. Another possibility is that OPA is specialized for walking only, since walking and crawling are different kinds of locomotion. To test these possibilities, we measured the responses in OPA to first-person perspective videos from both "walking" and "crawling" perspectives as well as for 2 conditions by which humans do not navigate ("flying" and "scrambled"). We found that OPA responded more to walking videos than to any of the others, including crawling, and did not respond more to crawling videos than to flying or scrambled ones. These results (i) reveal that OPA represents visual information only from a walking (not crawling) perspective, (ii) suggest crawling is processed by a different neural system, and (iii) raise questions for how OPA develops; namely, OPA may have never supported crawling, which is consistent with the hypothesis that OPA undergoes protracted development.

Topology of the lateral visual system: The fundus of the superior temporal sulcus and parietal area H connect nonvisual cerebrum to the lateral occipital lobe.

BACKGROUND AND PURPOSE: Mapping the topology of the visual system is critical for understanding how complex cognitive processes like reading can occur. We aim to describe the connectivity of the visual system to understand how the cerebrum accesses visual information in the lateral occipital lobe. METHODS: Using meta-analytic software focused on task-based functional MRI studies, an activation likelihood estimation (ALE) of the visual network was created. Regions of interest corresponding to the cortical parcellation scheme previously published under the Human Connectome Project were co-registered onto the ALE to identify the hub-like regions of the visual network. Diffusion Spectrum Imaging-based fiber tractography was performed to determine the structural connectivity of these regions with extraoccipital cortices. RESULTS: The fundus of the superior temporal sulcus (FST) and parietal area H (PH) were identified as hub-like regions for the visual network. FST and PH demonstrated several areas of coactivation beyond the occipital lobe and visual network. Furthermore, these parcellations were highly interconnected with other cortical regions throughout extraoccipital cortices related to their nonvisual functional roles. A cortical model demonstrating connections to these hub-like areas was created. CONCLUSIONS: FST and PH are two hub-like areas that demonstrate extensive functional coactivation and structural connections to nonvisual cerebrum. Their structural interconnectedness with language cortices along with the abnormal activation of areas commonly located in the temporo-occipital region in dyslexic individuals suggests possible important roles of FST and PH in the integration of information related to language and reading. Future studies should refine our model by examining the functional roles of these hub areas and their clinical significance.

Disturbances in primary visual processing as a function of healthy aging.

For decades, visual entrainment paradigms have been widely used to investigate basic visual processing in healthy individuals and those with neurological disorders. While healthy aging is known to be associated with alterations in visual processing, whether this extends to visual entrainment responses and the precise cortical regions involved is not fully understood. Such knowledge is imperative given the recent surge in interest surrounding the use of flicker stimulation and entrainment in the context of identifying and treating Alzheimer's disease (AD). In the current study, we examined visual entrainment in eighty healthy aging adults using magnetoencephalography (MEG) and a 15 Hz entrainment paradigm, while controlling for age-related cortical thinning. MEG data were imaged using a time-frequency resolved beamformer and peak voxel time series were extracted to quantify the oscillatory dynamics underlying the processing of the visual flicker stimuli. We found that, as age increased, the mean amplitude of entrainment responses decreased and the latency of these responses increased. However, there was no effect of age on the trial-to-trial consistency in phase (i.e., inter-trial phase locking) nor amplitude (i.e., coefficient of variation) of these visual responses. Importantly, we discovered that the relationship between age and response amplitude was fully mediated by the latency of visual processing. These results indicate that aging is associated with robust changes in the latency and amplitude of visual entrainment responses within regions surrounding the calcarine fissure, which should be considered in studies examining neurological disorders such as AD and other conditions associated with increased age.