Parahippocampal Place Area Activity Research Articles

From vision to memory: How scene-sensitive regions support episodic memory formation during child development

Previous brain imaging studies have identified three brain regions that selectively respond to visual scenes, the parahippocampal place area (PPA), the occipital place area (OPA), and the retrosplenial cortex (RSC). There is growing evidence that these visual scene-sensitive regions process different types of scene information and may have different developmental timelines in supporting scene perception. How these scene-sensitive regions support memory functions during child development is largely unknown. We investigated PPA, OPA and RSC activations associated with episodic memory formation in childhood (5–7 years of age) and young adulthood, using a subsequent scene memory paradigm and a functional localizer for scenes. PPA, OPA, and RSC subsequent memory activation and functional connectivity differed between children and adults. Subsequent memory effects were found in activations of all three scene regions in adults. In children, however, robust subsequent memory effects were only found in the PPA. Functional connectivity during successful encoding was significant among the three regions in adults, but not in children. PPA subsequently memory activations and PPA-RSC subsequent memory functional connectivity correlated with accuracy in adults, but not children. These age-related differences add new evidence linking protracted development of the scene-sensitive regions to the protracted development of episodic memory.

“Scene” from inside: The representation of Observer’s space in high-level visual cortex

Human observers are remarkably adept at perceiving and interacting with visual stimuli around them. Compared to visual stimuli like objects or faces, scenes are unique in that they provide enclosures for observers. An observer looks at a scene by being physically inside the scene. The current research explored this unique observer-scene relationship by studying the neural representation of scenes' spatial boundaries. Previous studies hypothesized that scenes' boundaries were processed in sets of high-level visual cortices. Notably, the parahippocampal place area (PPA), exhibited neural sensitivity to scenes that had closed vs. open spatial boundaries (Kravitz et al., 2011; Park et al., 2011). We asked whether this sensitivity reflected the openness of landscape (e.g., forest vs. beach), or the openness of the environment immediately surrounding the observer (i.e., whether a scene was viewed from inside vs. outside a room). Across two human fMRI experiments, we found that the PPA, as well as another well-known navigation-processing area, the occipital place area (OPA), processed scenes' boundaries according to the observer's space rather than the landscape. Moreover, we found that the PPA's activation pattern was susceptible to manipulations involving mid-level perceptual properties of scenes (e.g., rectilinear pattern of window frames), while the OPA's response was not. Our results have important implications for research in visual scene processing and suggest an important role of an observer's location in representing the spatial boundary, beyond the low-level visual input of a landscape.

The neural mechanisms underlying the maintenance of visual working memory contents

Visual working memory (WM) refers to the maintenance and manipulation of visual information that is not in the visual field. Visual WM provides an essential connection between perception and higher cognitive functions. Previous fMRI studies with classification methods showed that early visual cortex could retain information of visual features maintained in WM. However, we still know little about the neural mechanisms of visual WM during maintenance period in higher visual cortex and the influence of memory load on such mechanisms. Therefore, the present study utilized a modified delayed match-to-sample paradigm to investigate the visual WM performance. Participants were required to maintain one or two target items (face or house) for 11s. At the same time, function magnetic resonance imaging (fMRI) was applied to acquire the neural activities in visual cortical areas. Behavioral results showed that memory load but not stimuli significantly affected the accuracy of memory. Next, the amplitude of the neural activity during maintenance in each area was extracted. In order to reveal the areas sensitive to mnemonic stimuli, we compared the activity induced by face and house WM. The results showed that parahippocampal place area (PPA) and intra-parietal sulcus (IPS) were activated differently to different stimuli. Specifically, the neural response was stronger when house relative to face was held in memory. To further investigate whether other areas also retained visual information in WM, activation pattern analysis with decoding method was applied to the neural response in each area. The results demonstrated decoding performance in face selective areas including superior temporal sulcus (STS), FFA and V4. Taken together, these results indicated that higher visual cortex could retain visual information held in WM. Specifically, PPA and IPS showed general stronger responses to mnemonic houses than mnemonic faces, while FFA, STS, and V4 contained different detailed representations of mnemonic faces and mnemonic houses. These findings were consistent with previous findings concerning visual features, and supported the view that the contents in visual working memory are represented in visual cortex. Notably, we did not find any effects of memory load on the neural activity in PPA and IPS. However, the activity pattern analysis about other areas showed significant effects only in high memory load condition, suggesting that high memory load might refine the representations in face selective areas without boosting the average activation level. In order to find the cortical areas of which responses were significantly modulated by memory load, we further performed a voxel-based whole brain analysis. Specifically, a 2 (stimuli: face, house) * 2 (memory load: 1 item, 2 items) repeated measures ANOVA was performed for each voxel on the neural response during the maintenance. No interaction was observed in each voxel. Interestingly, the main effect for memory load was significant in bilateral putamen. In summary, our findings revealed the crucial role of higher visual cortex in maintaining visual information in WM and the important role of putamen in modulating memory load.

Schizophrenia and Category-Selectivity in the Brain: Normal for Faces but Abnormal for Houses.

Face processing is regularly found to be impaired in schizophrenia (SZ), thus suggesting that social malfunctioning might be caused by dysfunctional face processing. Most studies focused on emotional face processes, whereas non-emotional face processing received less attention. While current reports on abnormal face processing in SZ are mixed, examinations of non-emotional face processing compared to adequate control stimuli may clarify whether SZ is characterized by a face-processing deficit. Patients with SZ (n = 28) and healthy controls (n = 30) engaged in an fMRI scan where images of non-emotional faces and houses were presented. A simple inverted-picture detection task warranted the participants’ attention. Region of interest (ROI) analyses were conducted on face-sensitive regions including the fusiform face area, the occipital face area, and the superior temporal sulcus. Scene-sensitivity was assessed in the parahippocampal place area (PPA) and served as control condition. Patients did not show aberrant face-related neural processes in face-sensitive regions. This finding was also evident when analyses were done on individually defined ROIs or on in-house-localizer ROIs. Patients revealed a decreased specificity toward house stimuli as reflected in decreased neural response toward houses in the PPA. Again, this result was supported by supplementary analyses. Neural activation toward neutral faces was not found to be impaired in SZ, therefore speaking against an overall face-processing deficit. Aberrant activation in scene-sensitive PPA is also found in assessments of memory processes in SZ. It is up to future studies to show how impairments in PPA relate to functional outcome in SZ.

Conjoint representation of texture ensemble and location in the parahippocampal place area.

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.

Perception of Impossible Scenes Reveals Differential Hippocampal and Parahippocampal Place Area Contributions to Spatial Coherency.

Surprisingly little is known about how the brain combines spatial elements to form a coherent percept. Regions that may underlie this process include the hippocampus (HC) and parahippocampal place area (PPA), regions central to spatial perception but whose role in spatial coherency has not been explored. Participants were scanned with functional MRI while they judged whether Escher-like scenes were possible or impossible. Univariate analyses revealed differential HC and PPA involvement, with greater HC activity during spatial incoherency detection and more PPA activity during spatial coherency detection. Recognition and eye-tracking data ruled out long- or short-term memory confounds. Multivariate statistics demonstrated spatial coherency-dependent functional connectivity for the HC, but not PPA, with greater HC connectivity to various brain regions including lateral occipital complex during spatial incoherency detection. We suggest the PPA is preferentially involved during the perception of spatially coherent scenes, whereas the HC binds distinct features to create coherent representations. © 2016 Wiley Periodicals, Inc.

FMRI neurofeedback of higher visual areas and perceptual biases

The self-regulation of brain activation via neurofeedback training offers a method to study the relationship between brain areas and perception in a more direct manner than the conventional mapping of brain responses to different types of stimuli. The current proof-of-concept study aimed to demonstrate that healthy volunteers can self-regulate activity in the parahippocampal place area (PPA) over the fusiform face area (FFA). Both areas are involved in higher order visual processing and are activated during the imagery of scenes and faces respectively. Participants (N=9) were required to upregulate PPA relative to FFA activity, and all succeeded at the task, with imagery of scenes being the most commonly reported mental strategy. A control group (N=8) underwent the same imagery and testing procedure, albeit without neurofeedback, in a mock MR scanner to account for any non-specific training effects. The upregulation of PPA activity occurred concurrently with activation of prefrontal and parietal areas, which have been associated with ideation and mental image generation. We tested whether successful upregulation of the PPA relative to FFA had consequences on perception by assessing bistable perception of faces and houses in a binocular rivalry task (before and after the scanning sessions) and categorisation of faces and scenes presented in transparent composite images (during scanning, interleaved with the self-regulation blocks). Contrary to our expectations, upregulation of the PPA did not alter the duration of face or house perception in the rivalry task and response speed and accuracy in the categorisation task. This conclusion was supported by the results of another control experiment (N=10 healthy participants) that involved intensive exposure to category-specific stimuli and did not show any behavioural or perceptual changes. We conclude that differential self-regulation of higher visual areas can be achieved, but that perceptual biases under conditions of stimulus rivalry are relatively robust against such internal modulation of localised brain activity. This study sets the basis for future investigations of perceptual and behavioural consequences of localised self-regulation of neural activity.

Spatial frequency processing in scene-selective cortical regions

Visual analysis begins with the parallel extraction of different attributes at different spatial frequencies. Low spatial frequencies (LSF) convey coarse information and are characterized by high luminance contrast, while high spatial frequencies (HSF) convey fine details and are characterized by low luminance contrast. In the present fMRI study, we examined how scene-selective regions—the parahippocampal place area (PPA), the retrosplenial cortex (RSC) and the occipital place area (OPA)—responded to spatial frequencies when contrast was either equalized or not equalized across spatial frequencies. Participants performed a categorization task on LSF, HSF and non-filtered scenes belonging to two different categories (indoors and outdoors). We either left contrast across scenes untouched, or equalized it using a root-mean-square contrast normalization. We found that when contrast remained unmodified, LSF and NF scenes elicited greater activation than HSF scenes in the PPA. However, when contrast was equalized across spatial frequencies, the PPA was selective to HFS. This suggests that PPA activity relies on an interaction between spatial frequency and contrast in scenes. In the RSC, LSF and NF elicited greater response than HSF scenes when contrast was not modified, while no effect of spatial frequencies appeared when contrast was equalized across filtered scenes, suggesting that the RSC is sensitive to high-contrast information. Finally, we observed selective activation of the OPA in response to HSF, irrespective of contrast manipulation. These results provide new insights into how scene-selective areas operate during scene processing.

FMRI Investigation of Monocular Pattern Rivalry

In monocular pattern rivalry, a composite image is shown to both eyes. The patient experiences perceptual alternations in which the two stimulus components alternate in clarity or salience. We used fMRI at 3T to image brain activity while participants perceived monocular rivalry passively or indicated their percepts with a task. The stimulus patterns were left/right oblique gratings, face/house composites, or a nonrivalrous control stimulus that did not support the perception of transparency or image segmentation. All stimuli were matched for luminance, contrast, and color. Compared with the control stimulus, the cortical activation for passive viewing of grating rivalry included dorsal and ventral extrastriate cortex, superior and inferior parietal regions, and multiple sites in frontal cortex. When the BOLD signal for the object rivalry task was compared with the grating rivalry task, a similar whole-brain network was engaged, but with significantly greater activity in extrastriate regions, including V3, V3A, fusiform face area (FFA), and parahippocampal place area (PPA). In addition, for the object rivalry task, FFA activity was significantly greater during face-dominant periods whereas parahippocampal place area activity was greater during house-dominant periods. Our results demonstrate that slight stimulus changes that trigger monocular rivalry recruit a large whole-brain network, as previously identified for other forms of bistability. Moreover, the results indicate that rivalry for complex object stimuli preferentially engages extrastriate cortex. We also establish that even with natural viewing conditions, endogenous attentional fluctuations in monocular pattern rivalry will differentially drive object-category-specific cortex, similar to binocular rivalry, but without complete suppression of the nondominant image.

Affective scenes influence fear perception of individual body expressions.

In natural viewing conditions, different stimulus categories such as people, objects, and natural scenes carry relevant affective information that is usually processed simultaneously. But these different signals may not always have the same affective meaning. Using body-scene compound stimuli, we investigated how the brain processes fearful signals conveyed by either a body in the foreground or scenes in the background and the interaction between foreground body and background scene. The results showed that left and right extrastriate body areas (EBA) responded more to fearful than to neutral bodies. More interestingly, a threatening background scene compared to a neutral one showed increased activity in bilateral EBA and right-posterior parahippocampal place area (PPA) and decreased activity in right retrosplenial cortex (RSC) and left-anterior PPA. The emotional scene effect in EBA was only present when the foreground body was neutral and not when the body posture expressed fear (significant emotion-by-category interaction effect), consistent with behavioral ratings. The results provide evidence for emotional influence of the background scene on the processing of body expressions.

Functional imaging correlates of impaired distractor suppression following sleep deprivation

Sleep deprivation (SD) has been shown to affect selective attention but it is not known how two of its component processes: target enhancement and distractor suppression, are affected. To investigate, young volunteers either attended to houses or were obliged to ignore them (when attending to faces) while viewing superimposed face-house pictures. MR signal enhancement and suppression in the parahippocampal place area (PPA) were determined relative to a passive viewing control condition. Sleep deprivation was associated with lower PPA activation across conditions. Critically SD specifically impaired distractor suppression in selective attention, leaving target enhancement relatively preserved. These findings parallel some observations in cognitive aging. Additionally, following SD, attended houses were not significantly better recognized than ignored houses in a post-experiment test of recognition memory contrasting with the finding of superior recognition of attended houses in the well-rested state. These results provide evidence for co-encoding of distracting information with targets into memory when one is sleep deprived.

Neural indices of improved attentional modulation over middle childhood

The ability to control the focus of attention relies on top-down modulation of cortical activity in areas involved in stimulus processing, and this ability is critical for maintaining items in working memory in the presence of distraction. Prior research demonstrates that children are less capable of focusing attention, relative to adults, and that this ability develops significantly during middle childhood. Here, using fMRI and a face/scene working memory task adapted from Gazzaley and colleagues (Gazzaley et al. 2005), we compared top-down modulation in fifteen children (aged 8-13) and fifteen young adults (aged 19-26). Replicating prior results, in young adults, attention to scenes modulated activity in the parahippocampal place area (PPA). In addition, modulation of PPA activity increased as a function of age in children. PPA activity was also related to performance in this group, on the working memory task as well on a test of subsequent memory. Dorsolateral PFC also demonstrated increasing task-specific activation, as a function of age, in children. The present findings support the idea that children's reduced ability to maintain items in working memory, especially in the presence of distraction, is driven by weaker top-down modulation of activity in areas involved in stimulus processing.

Scene classification and parahippocampal place area activation in an individual with visual form agnosia

Scene classification and parahippocampal place area activation in an individual with visual form agnosia

Age differences in brain activity during perceptual versus reflective attention

This functional magnetic resonance imaging study presented participants with a face and scene simultaneously on each trial, and assessed the impact of perceptual versus reflective selective attention on activity in parahippocampal place area. Young and older adults showed equivalent activation in parahippocampal place area when cued to attend to the scene when the stimuli were perceptually present and when cued to refresh (briefly think about) the scene after the stimuli were no longer present. The groups also showed equivalent deactivation when cued to attend to the face when the stimuli were perceptually present. However, older adults showed less deactivation than young adults when cued to refresh the face, providing evidence for greater age-related disruption of reflective than perceptual selective attention.

Sleep Deprivation Impairs Object-Selective Attention: A View from the Ventral Visual Cortex

BackgroundMost prior studies on selective attention in the setting of total sleep deprivation (SD) have focused on behavior or activation within fronto-parietal cognitive control areas. Here, we evaluated the effects of SD on the top-down biasing of activation of ventral visual cortex and on functional connectivity between cognitive control and other brain regions.Methodology/Principal FindingsTwenty-three healthy young adult volunteers underwent fMRI after a normal night of sleep (RW) and after sleep deprivation in a counterbalanced manner while performing a selective attention task. During this task, pictures of houses or faces were randomly interleaved among scrambled images. Across different blocks, volunteers responded to house but not face pictures, face but not house pictures, or passively viewed pictures without responding. The appearance of task-relevant pictures was unpredictable in this paradigm. SD resulted in less accurate detection of target pictures without affecting the mean false alarm rate or response time. In addition to a reduction of fronto-parietal activation, attending to houses strongly modulated parahippocampal place area (PPA) activation during RW, but this attention-driven biasing of PPA activation was abolished following SD. Additionally, SD resulted in a significant decrement in functional connectivity between the PPA and two cognitive control areas, the left intraparietal sulcus and the left inferior frontal lobe.Conclusions/SignificanceSD impairs selective attention as evidenced by reduced selectivity in PPA activation. Further, reduction in fronto-parietal and ventral visual task-related activation suggests that it also affects sustained attention. Reductions in functional connectivity may be an important additional imaging parameter to consider in characterizing the effects of sleep deprivation on cognition.

The internal anticipation of sensory action effects: when action induces FFA and PPA activity

Voluntary action – in particular the ability to produce desired effects in the environment – is fundamental to human existence. According to ideomotor theory we can achieve goals in the environment by means of anticipating their outcomes. We aimed at providing neurophysiological evidence for the assumption that performing actions calls for the activation of brain areas associated with the sensory effects usually evoked by the actions. We conducted an fMRI study in which right and left button presses lead to the presentation of face and house pictures. We compared a baseline phase with the same phase after participants experienced the association between button presses and pictures. We found an increase in the parahippocampal place area (PPA) for the response that has been associated with house pictures and fusiform face area (FFA) for the response that has been coupled with face pictures. This observation constitutes support for ideomotor theory.

Continuous mapping of the cortical object vision pathway using traveling waves in object space

Research into the organization of high-level visual cortex has mainly used discrete object classes (e.g. faces and buildings). In contrast, the lower levels of the visual cortex have mainly been studied using phase-encoding techniques with gradually changing rotating wedges and expanding/contracting rings. The gradual stimulus changes cause traveling waves on the cortical surface and time delays of each cortical location are related to stimulus preference. We propose to extend this method to study higher-order properties of visual objects. We created gradual morphing sequences from a face into a building and vice versa. The activation in traditional face- and house-selective regions corresponding to fusiform face area (FFA) and parahippocampal place area (PPA) was time-locked to presentation of respectively face(-like) and building(-like) stimuli in the morphing sequences. We also included contracting/expanding rings containing images of parts of natural scenes. Confirming existing literature with discrete object classes, activity in FFA and PPA was time-locked to the presentation of foveal and eccentric rings, respectively. The results however contradict large-scale continuous maps across the ventral visual stream, as the cortical area between FFA and PPA was not modulated by the position in the morphing sequences, or by the retinotopic position of the rings. We conclude that phase-encoding techniques can help in revealing the organization of high-level visual regions for complex object properties.

Sleep deprivation and its effects on object-selective attention

Sleep deprivation (SD) affects attention but it is an open question as to whether all subtypes of attention are similarly affected. We investigated the effects of 24 h of total SD on object-selective attention. 26 healthy, young adults viewed quartets of alternating faces or place scenes and performed selective judgments on faces only, scenes only or both faces and scenes. Volunteers underwent fMRI following a normal night of sleep and again following approximately 24 h of total sleep deprivation in a counterbalanced fashion. Sleep deprivation resulted in slower and less accurate picture classification as well as poorer recognition memory for scenes. Attention strongly modulated activation in the Parahippocampal Place Area (PPA). Task-related activation in the fronto-parietal cortex and PPA was reduced in SD, but the relative modulation of PPA activation by attention was preserved. Psychophysiological interaction between the left intra-parietal sulcus and the PPA that was clearly present after a normal night of sleep was reduced below threshold following SD suggesting that PPI may be a more sensitive method of detecting change in selective attention. Sleep deprivation may affect object-selective attention in addition to exerting a task-independent deficit in attention.

Full Scenes produce more activation than Close-up Scenes and Scene-Diagnostic Objects in parahippocampal and retrosplenial cortex: An fMRI study

We used fMRI to directly compare activation in two cortical regions previously identified as relevant to real-world scene processing: retrosplenial cortex and a region of posterior parahippocampal cortex functionally defined as the parahippocampal place area (PPA). We compared activation in these regions to full views of scenes from a global perspective, close-up views of sub-regions from the same scene category, and single objects highly diagnostic of that scene category. Faces were included as a control condition. Activation in parahippocampal place area was greatest for full scene views that explicitly included the 3D spatial structure of the environment, with progressively less activation for close-up views of local scene regions containing diagnostic objects but less explicitly depicting 3D scene geometry, followed by single scene-diagnostic objects. Faces did not activate parahippocampal place area. In contrast, activation in retrosplenial cortex was greatest for full scene views, and did not differ among close-up views, diagnostic objects, and faces. The results showed that parahippocampal place area responds in a graded fashion as images become more completely scene-like and include more explicit 3D structure, whereas retrosplenial cortex responds in a step-wise manner to the presence of a complete scene. These results suggest scene processing areas are particularly sensitive to the 3D geometric structure that distinguishes scenes from other types of complex and meaningful visual stimuli.

Where Am I Now? Distinct Roles for Parahippocampal and Retrosplenial Cortices in Place Recognition

A key component of spatial navigation is the ability to use visual information to ascertain where one is located and how one is oriented in the world. We used functional magnetic resonance imaging to examine the neural correlates of this phenomenon in humans. Subjects were scanned while retrieving different kinds of topographical and nontopographical information in response to visual scenes. In the three critical conditions, they viewed images of a familiar college campus, and reported either the location of the place depicted in the image (location task), the compass direction that the camera was facing when the image was taken (orientation task), or whether the location was on campus or not (familiarity task). Our analyses focused on the retrosplenial cortex (RSC)/parietal-occipital sulcus region and the parahippocampal place area (PPA), which previous studies indicate play a critical role in place recognition. RSC activity depended on the type of information retrieved, with the strongest response in the location task. In contrast, PPA activity did not depend on the retrieval task. Additional analyses revealed a strong effect of familiarity in RSC but not in the PPA, with the former region responding much more strongly to images of the familiar campus than to images of an unfamiliar campus. These results suggest that the PPA and RSC play distinct but complementary roles in place recognition. In particular, the PPA may primarily support perception of the immediate scene, whereas RSC may support memory retrieval mechanisms that allow the scene to be localized within the broader spatial environment.