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      Architecture of the brain’s visual system enhances network stability and performance through layers, delays, and feedback

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          In the visual system of primates, image information propagates across successive cortical areas, and there is also local feedback within an area and long-range feedback across areas. Recent findings suggest that the resulting temporal dynamics of neural activity are crucial in several vision tasks. In contrast, artificial neural network models of vision are typically feedforward and do not capitalize on the benefits of temporal dynamics, partly due to concerns about stability and computational costs.

          In this study, we focus on recurrent networks with feedback connections for visual tasks with static input corresponding to a single fixation. We demonstrate mathematically that a network’s dynamics can be stabilized by four key features of biological networks: layer-ordered structure, temporal delays between layers, longer distance feedback across layers, and nonlinear neuronal responses. Conversely, when feedback has a fixed distance, one can omit delays in feedforward connections to achieve more efficient artificial implementations.

          We also evaluated the effect of feedback connections on object detection and classification performance using standard benchmarks, specifically the COCO and CIFAR10 datasets. Our findings indicate that feedback connections improved the detection of small objects, and classification performance became more robust to noise. We found that performance increased with the temporal dynamics, not unlike what is observed in core vision of primates.

          These results suggest that delays and layered organization are crucial features for stability and performance in both biological and artificial recurrent neural networks.

          Author summary

          The visual cortex is a part of the brain that receives, integrates, and processes visual information. It is made up of many interconnected areas that work together to help us see. Studies have shown that lateral and feedback connections between these areas are essential for us to be able to see and understand the world around us. However, most computer vision models only consider feedforward connections.

          In this study, we looked at the stability of networks with feedback. We used mathematical tools to discover that layered networks with long-range feedback favor stability, as do biologically realistic implementations with temporal delays in the feedforward connections. We also demonstrated the performance advantages of adding feedback connections to convolutional networks in image classification and detection tasks.

          These results suggest that the organization of the visual system favors stability. This implies that biologically more realistic implementations of computational vision networks may be easier to train.

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          Most cited references50

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          The organization of the human cerebral cortex estimated by intrinsic functional connectivity.

          Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.
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            Complex brain networks: graph theoretical analysis of structural and functional systems.

            Recent developments in the quantitative analysis of complex networks, based largely on graph theory, have been rapidly translated to studies of brain network organization. The brain's structural and functional systems have features of complex networks--such as small-world topology, highly connected hubs and modularity--both at the whole-brain scale of human neuroimaging and at a cellular scale in non-human animals. In this article, we review studies investigating complex brain networks in diverse experimental modalities (including structural and functional MRI, diffusion tensor imaging, magnetoencephalography and electroencephalography in humans) and provide an accessible introduction to the basic principles of graph theory. We also highlight some of the technical challenges and key questions to be addressed by future developments in this rapidly moving field.
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              Backpropagation through time: what it does and how to do it

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput Biol
                plos
                PLOS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                November 2023
                10 November 2023
                : 19
                : 11
                : e1011078
                Affiliations
                [1 ] Biomedical Engineering Department, The City College of New York, New York, New York, United States of America
                [2 ] Levich Institute and Physics Department, The City College of New York, New York, New York, United States of America
                Brown University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-7291-4018
                Article
                PCOMPBIOL-D-23-00540
                10.1371/journal.pcbi.1011078
                10664920
                37948463
                d92ab950-15a7-4ce2-ada9-48ca1dccea5b
                © 2023 Velarde et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 April 2023
                : 19 October 2023
                Page count
                Figures: 12, Tables: 2, Pages: 27
                Funding
                Funded by: NIH
                Award ID: R01CA247910
                Award Recipient :
                This work was supported by NIH grant R01CA247910 (LCP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                2023-11-22
                All relevant data are within the manuscript and its Supporting information file.

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