Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network

International audienceSpatial navigation involves multiple cognitive processes including multisensory integration, visuospatial coding, memory, and decision-making. These functions are mediated by the interplay of cerebral structures that can be broadly separated into a posterior network (subserving visual and spatial processing) and an anterior network (dedicated to memory and navigation planning). Within these networks, areas such as the hippocampus (HC) are known to be affected by aging and to be associated with cognitive decline and navigation impairments. However, age-related changes in brain connectivity within the spatial navigation network remain to be investigated. For this purpose, we performed a neuroimaging study combining functional and structural connectivity analyses between cerebral regions involved in spatial navigation. Nineteen young (μ = 27 years, σ = 4.3; 10 F) and 22 older (μ = 73 years, σ = 4.1; 10 F) participants were examined in this study. Our analyses focused on the parahippocampal place area (PPA), the retrosplenial cortex (RSC), the occipital place area (OPA), and the projections into the visual cortex of central and peripheral visual fields, delineated from independent functional localizers. In addition, we segmented the HC and the medial prefrontal cortex (mPFC) from anatomical images. Our results show an age-related decrease in functional connectivity between low-visual areas and the HC, associated with an increase in functional connectivity between OPA and PPA in older participants compared to young subjects. Concerning the structural connectivity, we found age-related differences in white matter integrity within the navigation brain network, with the exception of the OPA. The OPA is known to be involved in egocentric navigation, as opposed to allocentric strategies which are more related to the hippocampal region. The increase in functional connectivity between the OPA and PPA may thus reflect a compensatory mechanism for the age-related alterations around the HC, favoring the use of the preserved structural network mediating egocentric navigation. Overall, these findings on age-related differences of functional and structural connectivity may help to elucidate the cerebral bases of spatial navigation deficits in healthy and pathological aging

Mobile brain/body imaging of landmark‐based navigation with high‐density EEG

Coupling behavioral measures and brain imaging in naturalistic, ecological conditions is key to comprehend the neural bases of spatial navigation. This highly integrative function encompasses sensorimotor, cognitive, and executive processes that jointly mediate active exploration and spatial learning. However, most neuroimaging approaches in humans are based on static, motion-constrained paradigms and they do not account for all these processes, in particular multisensory integration. Following the Mobile Brain/Body Imaging approach, we aimed to explore the cortical correlates of landmark-based navigation in actively behaving young adults, solving a Y-maze task in immersive virtual reality. EEG analysis identified a set of brain areas matching state-of-the-art brain imaging literature of landmark-based navigation. Spatial behavior in mobile conditions additionally involved sensorimotor areas related to motor execution and proprioception usually overlooked in static fMRI paradigms. Expectedly, we located a cortical source in or near the posterior cingulate, in line with the engagement of the retrosplenial complex in spatial reorientation. Consistent with its role in visuo-spatial processing and coding, we observed an alpha-power desynchronization while participants gathered visual information. We also hypothesized behavior-dependent modulations of the cortical signal during navigation. Despite finding few differences between the encoding and retrieval phases of the task, we identified transient time-frequency patterns attributed, for instance, to attentional demand, as reflected in the alpha/gamma range, or memory workload in the delta/theta range. We confirmed that combining mobile high-density EEG and biometric measures can help unravel the brain structures and the neural modulations subtending ecological landmark-based navigation

The neural bases of spatial frequency processing during scene perception

International audienceTheories on visual perception agree that scenes are processed in terms of spatial frequencies. Low spatial frequencies (LSF) carry coarse information whereas high spatial frequencies (HSF) carry fine details of the scene. However, how and where spatial frequencies are processed within the brain remain unresolved questions. The present review addresses these issues and aims to identify the cerebral regions differentially involved in low and high spatial frequency processing, and to clarify their attributes during scene perception. Results from a number of behavioral and neuroimaging studies suggest that spatial frequency processing is lateralized in both hemispheres, with the right and left hemispheres predominantly involved in the categorization of LSF and HSF scenes, respectively. There is also evidence that spatial frequency processing is retinotopically mapped in the visual cortex. HSF scenes (as opposed to LSF) activate occipital areas in relation to foveal representations, while categorization of LSF scenes (as opposed to HSF) activates occipital areas in relation to more peripheral representations. Concomitantly, a number of studies have demonstrated that LSF information may reach high-order areas rapidly, allowing an initial coarse parsing of the visual scene, which could then be sent back through feedback into the occipito-temporal cortex to guide finer HSF-based analysis. Finally, the review addresses spatial frequency processing within scene-selective regions areas of the occipito-temporal cortex

Variance-dependent neural activity in an unvoluntary averaging task

International audienceEnsemble statistics of a visual scene can be estimated to provide a gist of the scene without detailed analysis of all individual items. The simplest and most widely studied ensemble statistic is mean estimation, which requires averaging an ensemble of elements. Averaging is useful to estimate the mean of an ensemble and discard the variance. The source of variance can be external (i.e., variance across the physical elements) or internal (i.e., imprecisions in the estimates of the elements by the visual system). The equivalent noise paradigm is often used to measure the impact of the internal variance (i.e., the equivalent input noise). This paradigm relies on the assumption that the averaging process is equally effective independently of the main source of variance, internal or external, so any difference between the processing when the main source of variance is internal or external must be assumed not to affect the averaging efficiency. The current fMRI study compared the neural activity when the main variance is caused by the stimulus (i.e., high variance) and when it is caused by imprecisions in the estimates of the elements by the visual system (i.e., low variance). The results showed that the right superior frontal and left middle frontal gyri can be significantly more activated when the variance in the orientation of the Gabors was high than when it was low. Consequently, the use of the equivalent noise paradigm requires the assumption that such additional neural activity in high variance does not affect the averaging efficiency

Differential Brain Activity in Regions Linked to Visuospatial Processing During Landmark-Based Navigation in Young and Healthy Older Adults

International audienceOlder adults have difficulties in navigating unfamiliar environments and updating their wayfinding behavior when faced with blocked routes. This decline in navigational capabilities has traditionally been ascribed to memory impairments and dysexecutive function, whereas the impact of visual aging has often been overlooked. The ability to perceive visuospatial information such as salient landmarks is essential to navigating efficiently. To date, the functional and neurobiological factors underpinning landmark processing in aging remain insufficiently characterized. To address this issue, functional magnetic resonance imaging (fMRI) was used to investigate the brain activity associated with landmark-based navigation in young and healthy older participants. The performances of 25 young adults (μ = 25.4 years, σ = 2.7; seven females) and 17 older adults (μ = 73.0 years, σ = 3.9; 10 females) were assessed in a virtual-navigation task in which they had to orient using salient landmarks. The underlying whole-brain patterns of activity as well as the functional roles of specific cerebral regions involved in landmark processing, namely the parahippocampal place area (PPA), the occipital place area (OPA), and the retrosplenial cortex (RSC), were analyzed. Older adults' navigational abilities were overall diminished compared to young adults. Also, the two age groups relied on distinct navigational strategies to solve the task. Better performances during landmark-based navigation were associated with increased neural activity in an extended neural network comprising several cortical and cerebellar regions. Direct comparisons between age groups revealed that young participants had greater anterior temporal activity. Also, only young adults showed significant activity in occipital areas corresponding to the cortical projection of the central visual field during landmark-based navigation. The region-of-interest analysis revealed an increased OPA activation in older adult participants during the landmark condition. There were no significant between-group differences in PPA and RSC activations. These preliminary results hint at the possibility that aging diminishes fine-grained information processing in occipital and temporal regions, thus hindering the capacity to use landmarks adequately for navigation. Keeping sight of its exploratory nature, this work helps towards a better comprehension of the neural dynamics subtending landmark-based navigation and it provides new insights on the impact of age-related visuospatial processing differences on navigation capabilities

Age-Related Differences in Spatial Frequency Processing during Scene Categorization.

Visual analysis of real-life scenes starts with the parallel extraction of different visual elementary features at different spatial frequencies. The global shape of the scene is mainly contained in low spatial frequencies (LSF), and the edges and borders of objects are mainly contained in high spatial frequencies (HSF). The present fMRI study investigates the effect of age on the spatial frequency processing in scenes. Young and elderly participants performed a categorization task (indoor vs. outdoor) on LSF and HSF scenes. Behavioral results revealed performance degradation for elderly participants only when categorizing HSF scenes. At the cortical level, young participants exhibited retinotopic organization of spatial frequency processing, characterized by medial activation in the anterior part of the occipital lobe for LSF scenes (compared to HSF), and the lateral activation in the posterior part of the occipital lobe for HSF scenes (compared to LSF). Elderly participants showed activation only in the anterior part of the occipital lobe for LSF scenes (compared to HSF), but not significant activation for HSF (compared to LSF). Furthermore, a ROI analysis revealed that the parahippocampal place area, a scene-selective region, was less activated for HSF than LSF for elderly participants only. Comparison between groups revealed greater activation of the right inferior occipital gyrus in young participants than in elderly participants for HSF. Activation of temporo-parietal regions was greater in elderly participants irrespective of spatial frequencies. The present findings indicate a specific low-contrasted HSF deficit for normal elderly people, in association with an occipito-temporal cortex dysfunction, and a functional reorganization of the categorization of filtered scenes

Does RMS contrast normalization impair Coarse-to-Fine processing of natural scenes?

International audienceVisual analysis starts with the parallel extraction of different attributes at different spatial frequencies (SF) following a predominant and default coarse-to-fine processing sequence. Low spatial frequencies (LSF) would be processed faster than high spatial frequencies (HSF), allowing an initial coarse parsing of the visual input, before the analysis of the finer information. Studies investigating SF processing commonly use SF-filtered images as stimuli. Since LSF and HSF differ not only in terms of SF, but also in terms of luminance and contrast, recent studies normalized RMS contrast of images (i.e. the standard deviation of luminance values) in order to avoid any confound between SF components and known effects of luminance and contrast.In the present study, we investigated whether RMS contrast normalization of filtered scenes would induce bias in the default coarse-to-fine processing strategy during a categorization task (indoor vs. outdoor). We used dynamic sequences as stimuli composed of bandpass-filtered versions of a scene, presented from LSF to HSF or from HSF to LSF, allowing us to impose a coarse-to-fine (CtF) or a fine-to-coarse (FtC) processing of the scenes. In one condition (LUM), only the mean luminance of the filtered scenes was equated. In the other condition (RMS), both the mean luminance and the RMS contrast were equalized across the filtered scenes. In the LUM condition, CtF sequences were categorized faster than FtC sequences, consistent with a considerable number of studies. However, in the RMS condition, there was no advantage of CtF over FtC processing. The present study thus suggests that RMS contrast normalization of filtered scenes induces changes in the default SF processing strategies. We argue that such manipulation modify scene spectral properties that are exploited by the visual system to enable recognition. RMS contrast normalization should thus be used with caution when investigating SF processing of natural scenes

Spatial frequency processing in scene-selective cortical regions

International audienceVisual 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

An Appraisal of the Role of the Neocerebellum for Spatial Navigation in Healthy Aging

International audienceSpatial navigation is an intricate ability, requiring multisensory and motor integration, that is particularly impacted in aging. The age-related decline in navigational capabilities is known to be associated with changes in brain regions such as the frontal, temporal, and cerebellar cortices. Age-related cerebellar differences in spatial navigation have generally been ascribed to motor impairments, omitting the central role of this structure in several cognitive processes. In the present voxel-based morphometric study, we investigated gray matter volume loss in older adults across cognitive and motor subregions of the cerebellum. Specifically, we hypothesized that age-related gray matter differences would occur mainly in cerebellar regions involved in cognitive processing. Our results showed a significant age-related atrophy in the left neocerebellum of healthy older adults that includes Crus I and lobule VI. The latter are important nodes in the network that subtends cognitive abilities such as object recognition and spatial cognition. This exploratory work sets the ground for future research to investigate the extent of the neocerebellum's contribution to spatial navigation deficits in aging

Scene perception in age-related macular degeneration: Effect of spatial frequencies and contrast in residual vision

International audienceAge-related macular degeneration (AMD) is characterized by a central vision loss. Here, we investigated the ability of AMD patients to process the spatial frequency content of scenes in their residual vision, depending of the luminance contrast level. AMD patients and normally-sighted elderly participants (controls) performed a categorization task involving large scenes (outdoors vs. indoors) filtered in low spatial frequencies (LSF), high spatial frequencies (HSF), and non-filtered scenes (NF). Luminance contrast of scenes was equalized between stimuli using a root-mean square (RMS) contrast normalization. In Experiment 1, we applied an RMS contrast of 0.1 (for luminance values between 0 and 1), a value situated between the mean contrast of LSF and HSF scenes in natural conditions. In Experiment 2, we applied an RMS contrast of 0.3, corresponding to the mean contrast of HSF scenes in natural conditions. In Experiment 3, we manipulated four levels of linearly-increasing RMS contrasts (0.05, 0.10, 0.15, and 0.20) for HSF scenes only. Compared to controls, AMD patients gave more non-responses in the categorization of HSF than NF or LSF scenes, irrespective of the contrast level of scenes. Performances improved as contrast increased in HSF scenes. Controls were not differentially affected by the spatial frequency content of scenes. Overall, results suggest that LSF processing is well preserved in AMD patients and allows efficient scene categorization in their parafoveal residual vision. The HSF processing deficit could be partially restored by enhancing luminance contrast