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The distinct and overlapping brain networks supporting semantic and spatial constructive scene processing.

ABSTRACT: Scene imagery features prominently when we recall autobiographical memories, imagine the future and navigate around in the world. Consequently, in this study we sought to better understand how scene representations are supported by the brain. Processing scenes involves a variety of cognitive processes that in the real world are highly interactive. Here, however, our goal was to separate semantic and spatial constructive scene processes in order to identify the brain areas that were distinct to each process, those they had in common, and the connectivity between regions. To this end, participants searched for either semantic or spatial constructive impossibilities in scenes during functional MRI. We focussed our analyses on only those scenes that were possible, thus removing any error detection that would evoke reactions such as surprise or novelty. Importantly, we also counterbalanced possible scenes across participants, enabling us to examine brain activity and connectivity for the same possible scene images under two different conditions. We found that participants adopted different cognitive strategies, which were reflected in distinct oculomotor behaviour, for each condition. These were in turn associated with increased engagement of lateral temporal and parietal cortices for semantic scene processing, the hippocampus for spatial constructive scene processing, and increased activation of the ventromedial prefrontal cortex (vmPFC) that was common to both. Connectivity analyses showed that the vmPFC switched between semantic and spatial constructive brain networks depending on the task at hand. These findings further highlight the well-known semantic functions of lateral temporal areas, while providing additional support for the previously-asserted contribution of the hippocampus to scene construction, and recent suggestions that the vmPFC may play a key role in orchestrating scene processing.

SUBMITTER: McCormick C

PROVIDER: S-EPMC8287593 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Introduction Post-traumatic stress disorder (PTSD) is associated with hippocampal system structural and functional impairments. Neurobiological models of PTSD posit that contextual memory for traumatic events is impaired due to hippocampal system dysfunction whilst memory of sensory details is enhanced due to amygdalar impact on sensory cortices. If hippocampal system dysfunction is a core feature of PTSD, then non-traumatic hippocampal-dependent cognitive functions such as scene construction, spatial processing, and memory should also be impaired in individuals with PTSD. Methods Forty-six trauma survivors, half diagnosed with PTSD, performed two tasks that involved spatial processing. The first was a scene construction task which requires conjuring-up spatially coherent multimodal scenarios, completed by all participants. Twenty-six participants (PTSD: n = 13) also completed a navigation task in a virtual environment, and underwent structural T1, T2 and diffusion-tensor MRI to quantify gray and white matter integrity. We examined the relationship between spatial processing, neural integrity, and symptom severity in a multiple factor analysis. Results Overall, patients with PTSD showed impaired performance in both tasks compared to controls. Scenes imagined by patients were less vivid, less detailed, and generated less sense of presence; importantly they had disproportionally reduced spatial coherence between details. Patients also made more errors during virtual navigation. Two components of the multiple factor analysis captured group differences. The first component explained 25% of the shared variance: participants that constructed less spatially coherent scenes also made more navigation errors and had reduced white matter integrity to long association tracts and tracts connecting the hippocampus, thalamus, and cingulate. The second component explained 20% of the variance: participants who generated fewer scene details, with less spatial coherence between them, had smaller hippocampal, parahippocampal and isthmus cingulate volumes. These participants also had increased white matter integrity to the right hippocampal cingulum bundle. Conclusion Our results suggest that patients with PTSD are impaired at imagining even neutral spatially coherent scenes and navigating through a complex spatial environment. Patients that showed reduced spatial processing more broadly had reduced hippocampal systems volumes and abnormal white matter integrity to tracts implicated in multisensory integration.

Project description:Higher-order cognitive processes were shown to rely on the interplay between large-scale neural networks. However, brain networks involved with the capability to split attentional resource over multiple spatial locations and multiple stimuli or sensory modalities have been largely unexplored to date. Here I re-analyzed data from Santangelo et al. (2010) to explore the causal interactions between large-scale brain networks during divided attention. During fMRI scanning, participants monitored streams of visual and/or auditory stimuli in one or two spatial locations for detection of occasional targets. This design allowed comparing a condition in which participants monitored one stimulus/modality (either visual or auditory) in two spatial locations vs. a condition in which participants monitored two stimuli/modalities (both visual and auditory) in one spatial location. The analysis of the independent components (ICs) revealed that dividing attentional resources across two spatial locations necessitated a brain network involving the left ventro- and dorso-lateral prefrontal cortex plus the posterior parietal cortex, including the intraparietal sulcus (IPS) and the angular gyrus, bilaterally. The analysis of Granger causality highlighted that the activity of lateral prefrontal regions were predictive of the activity of all of the posteriors parietal nodes. By contrast, dividing attention across two sensory modalities necessitated a brain network including nodes belonging to the dorsal frontoparietal network, i.e., the bilateral frontal eye-fields (FEF) and IPS, plus nodes belonging to the salience network, i.e., the anterior cingulated cortex and the left and right anterior insular cortex (aIC). The analysis of Granger causality highlights a tight interdependence between the dorsal frontoparietal and salience nodes in trials requiring divided attention between different sensory modalities. The current findings therefore highlighted a dissociation among brain networks implicated during divided attention across spatial locations and sensory modalities, pointing out the importance of investigating effective connectivity of large-scale brain networks supporting complex behavior.

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The distinct and overlapping brain networks supporting semantic and spatial constructive scene processing.

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