Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis

Perceived egocentric distance sensitivity and invariance across scene-selective cortex

The occipital place area represents the local elements of scenes

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.

The parahippocampal place area (PPA) is one of several brain regions that respond more strongly to scenes than to non-scene items such as objects and faces. The mechanism underlying this scene-preferential response remains unclear. One possibility is that the PPA is tuned to low-level stimulus features that are found more often in scenes than in less-preferred stimuli. Supporting this view, Nasr et al. (2014) recently observed that some of the stimuli that are known to strongly activate the PPA contain a large number of rectilinear edges. They further demonstrated that PPA response is modulated by rectilinearity for a range of non-scene images. Motivated by these results, we tested whether rectilinearity suffices to explain PPA selectivity for scenes. In the first experiment, we replicated the previous finding of modulation by rectilinearity in the PPA for arrays of 2-d shapes. However, two further experiments failed to find a rectilinearity effect for faces or scenes: high-rectilinearity faces and scenes did not activate the PPA any more strongly than low-rectilinearity faces and scenes. Moreover, the categorical advantage for scenes vs. faces was maintained in the PPA and two other scene-selective regions—the retrosplenial complex (RSC) and occipital place area (OPA)—when rectilinearity was matched between stimulus sets. We conclude that selectivity for scenes in the PPA cannot be explained by a preference for low-level rectilinear edges.

Spatial knowledge about an environment can be cued from memory by perception of a visual scene during active navigation or by imagination of the relationships between nonvisible landmarks, such as when providing directions. It is not known whether these different ways of accessing spatial knowledge elicit the same representations in the brain. To address this issue, we scanned participants with fMRI, while they performed a judgment of relative direction (JRD) task that required them to retrieve real-world spatial relationships in response to either pictorial or verbal cues. Multivoxel pattern analyses revealed several brain regions that exhibited representations that were independent of the cues to access spatial memory. Specifically, entorhinal cortex in the medial temporal lobe and the retrosplenial complex (RSC) in the medial parietal lobe coded for the heading assumed on a particular trial, whereas the parahippocampal place area (PPA) contained information about the starting location of the JRD. These results demonstrate the existence of spatial representations in RSC, ERC, and PPA that are common to visually guided navigation and spatial imagery.

Neural representation of scene boundaries

Texture provides crucial information about the category or identity of a scene. Nonetheless, not much is known about how the texture information in a scene is represented in the brain. Previous studies have shown that the parahippocampal place area (PPA), a scene-selective part of visual cortex, responds to simple patches of texture ensemble. However, in natural scenes textures exist in spatial context within a scene. Here we tested two hypotheses that make different predictions on how textures within a scene context are represented in the PPA. The Texture-Only hypothesis suggests that the PPA represents texture ensemble (i.e., the kind of texture) as is, irrespective of its location in the scene. On the other hand, the Texture and Location hypothesis suggests that the PPA represents texture and its location within a scene (e.g., ceiling or wall) conjointly. We tested these two hypotheses across two experiments, using different but complementary methods. In experiment 1, by using multivoxel pattern analysis (MVPA) and representational similarity analysis, we found that the representational similarity of the PPA activation patterns was significantly explained by the Texture-Only hypothesis but not by the Texture and Location hypothesis. In experiment 2, using a repetition suppression paradigm, we found no repetition suppression for scenes that had the same texture ensemble but differed in location (supporting the Texture and Location hypothesis). On the basis of these results, we propose a framework that reconciles contrasting results from MVPA and repetition suppression and draw conclusions about how texture is represented in the PPA.NEW & NOTEWORTHY This study investigates how the parahippocampal place area (PPA) represents texture information within a scene context. We claim that texture is represented in the PPA at multiple levels: the texture ensemble information at the across-voxel level and the conjoint information of texture and its location at the within-voxel level. The study proposes a working hypothesis that reconciles contrasting results from multivoxel pattern analysis and repetition suppression, suggesting that the methods are complementary to each other but not necessarily interchangeable.

The human entorhinal-hippocampal circuitry is characterized by an information-specific functional organization where two routes, that are preferentially connected to the parahippocampal cortex or the perirhinal and retrosplenial cortices, divide the entorhinal cortex as well as hippocampal subiculum and CA1 subregions.

Target objects required for goal-directed behavior are typically embedded within multiple irrelevant objects that may interfere with their encoding. Most neuroimaging studies of high-level visual cortex have examined the representation of isolated objects, and therefore, little is known about how surrounding objects influence the neural representation of target objects. To investigate the effect of different types of clutter on the distributed responses to target objects in high-level visual areas, we used fMRI and manipulated the type of clutter. Specifically, target objects (i.e., a face and a house) were presented either in isolation, in the presence of a homogeneous (identical objects from another category) clutter ("pop-out" display), or in the presence of a heterogeneous (different objects) clutter, while participants performed a target identification task. Using multivoxel pattern analysis (MVPA) we found that in the posterior fusiform object area a heterogeneous but not homogeneous clutter interfered with decoding of the target objects. Furthermore, multivoxel patterns evoked by isolated objects were more similar to multivoxel patterns evoked by homogenous compared with heterogeneous clutter in the lateral occipital and posterior fusiform object areas. Interestingly, there was no effect of clutter on the neural representation of the target objects in their category-selective areas, such as the fusiform face area and the parahippocampal place area. Our findings show that the variation among irrelevant surrounding objects influences the neural representation of target objects in the object general area, but not in object category-selective cortex, where the representation of target objects is invariant to their surroundings.

A number of regions in the human brain are known to be involved in processing natural scenes, but the field has lacked a unifying framework for understanding how these different regions are organized and interact. We provide evidence from functional connectivity and meta-analyses for a new organizational principle, in which scene processing relies upon two distinct networks that split the classically defined parahippocampal place area (PPA). The first network of strongly connected regions consists of the occipital place area/transverse occipital sulcus and posterior PPA, which contain retinotopic maps and are not strongly coupled to the hippocampus at rest. The second network consists of the caudal inferior parietal lobule, retrosplenial complex, and anterior PPA, which connect to the hippocampus (especially anterior hippocampus), and are implicated in both visual and nonvisual tasks, including episodic memory and navigation. We propose that these two distinct networks capture the primary functional division among scene-processing regions, between those that process visual features from the current view of a scene and those that connect information from a current scene view with a much broader temporal and spatial context. This new framework for understanding the neural substrates of scene-processing bridges results from many lines of research, and makes specific functional predictions.

Keeping oriented in the environment is a multifaceted ability that requires knowledge of at least three pieces of information: one’s own location (“place”) and orientation (“heading”) within the environment, and which location in the environment one is looking at (“view”). We used functional magnetic resonance imaging (fMRI) in humans to examine the neural signatures of these information. Participants were scanned while viewing snapshots which varied for place, view and heading within a virtual room. We observed adaptation effects, proportional to the physical distances between consecutive places and views, in scene-responsive (retrosplenial complex and parahippocampal gyrus), fronto-parietal and lateral occipital regions. Multivoxel pattern classification of signals in scene-responsive regions and in the hippocampus allowed supra-chance decoding of place, view and heading, and revealed the existence of map-like representations, where places and views closer in physical space entailed activity patterns more similar in neural representational space. The pattern of hippocampal activity reflected both view- and place-based distances, the pattern of parahippocampal activity preferentially discriminated between views, and the pattern of retrosplenial activity combined place and view information, while the fronto-parietal cortex only showed transient effects of changes in place, view, and heading. Our findings provide evidence for the presence of map-like spatial representations which reflect metric distances in terms of both one’s own and landmark locations.

Human adults flawlessly and effortlessly navigate boundaries and obstacles in the immediately visible environment, a process we refer to as guided navigation. Neuroimaging work in adults suggests this ability involves the occipital place area (OPA) [1, 2]-a scene-selective region in the dorsal stream that selectively represents information necessary for visually guided navigation [3-9]. Despite progress in understanding the neural basis of visually guided navigation, however, little is known about how this system develops. Is navigationally relevant information processing present in the first few years of life? Or does this information processing only develop after many years of experience? Although a handful of studies have found selective responses to scenes (relative to objects) in OPA in childhood [10-13], no study has explored how more specific navigationally relevant information processing emerges in this region. Here, we do just that by measuring OPA responses to first-person perspective motion information-a proxy for the visual experience of actually navigating the immediate environment-using fMRI in 5- and 8-year-old children. We found that, although OPA already responded more to scenes than objects by age 5, responses to first-person perspective motion were not yet detectable at this same age and rather only emerged by age 8. This protracted development was specific to first-person perspective motion through scenes, not motion on faces or objects, and was not found in other scene-selective regions (the parahippocampal place area or retrosplenial complex) or a motion-selective region (MT). These findings therefore suggest that navigationally relevant information processing in OPA undergoes prolonged development across childhood.

The Neurocognitive Basis of Spatial Reorientation

We used a multi-voxel classification analysis of functional magnetic resonance imaging (fMRI) data to determine to what extent item-specific information about complex natural scenes is represented in several category-selective areas of human extrastriate visual cortex during visual perception and visual mental imagery. Participants in the scanner either viewed or were instructed to visualize previously memorized natural scene exemplars, and the neuroimaging data were subsequently subjected to a multi-voxel pattern analysis (MVPA) using a support vector machine (SVM) classifier. We found that item-specific information was represented in multiple scene-selective areas: the occipital place area (OPA), parahippocampal place area (PPA), retrosplenial cortex (RSC), and a scene-selective portion of the precuneus/intraparietal sulcus region (PCu/IPS). Furthermore, item-specific information from perceived scenes was re-instantiated during mental imagery of the same scenes. These results support findings from previous decoding analyses for other types of visual information and/or brain areas during imagery or working memory, and extend them to the case of visual scenes (and scene-selective cortex). Taken together, such findings support models suggesting that reflective mental processes are subserved by the re-instantiation of perceptual information in high-level visual cortex. We also examined activity in the fusiform face area (FFA) and found that it, too, contained significant item-specific scene information during perception, but not during mental imagery. This suggests that although decodable scene-relevant activity occurs in FFA during perception, FFA activity may not be a necessary (or even relevant) component of one's mental representation of visual scenes.

IntroductionBrand equity plays a crucial role in a brand’s commercial success; however, research on the brain regions associated with brand equity has had mixed results. This study aimed to investigate key brain regions associated with the decision-making of branded and unbranded foods using quantitative neuroimaging meta-analysis and machine learning.MethodsQuantitative neuroimaging meta-analysis was performed using the activation likelihood method. Activation of the ventral medial prefrontal cortex (VMPFC) overlapped between branded and unbranded foods. The lingual and parahippocampal gyri (PHG) were activated in the case of branded foods, whereas no brain regions were characteristically activated in response to unbranded foods. We proposed a novel predictive method based on the reported foci data, referencing the multi-voxel pattern analysis (MVPA) results. This approach is referred to as the multi-coordinate pattern analysis (MCPA). We conducted the MCPA, adopting the sparse partial least squares discriminant analysis (sPLS-DA) to detect unique brain regions associated with branded and unbranded foods based on coordinate data. The sPLS-DA is an extended PLS method that enables the processing of categorical data as outcome variables.ResultsWe found that the lingual gyrus is a distinct brain region in branded foods. Thus, the VMPFC might be a core brain region in food categories in consumer behavior, regardless of whether they are branded foods. Moreover, the connection between the PHG and lingual gyrus might be a unique neural mechanism in branded foods.DiscussionAs this mechanism engages in imaging the feature-self based on emotionally subjective contextual associative memories, brand managers should create future-oriented relevancies between brands and consumers to build valuable brands.