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      Long-range population dynamics of anatomically defined neocortical networks


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          The coordination of activity across neocortical areas is essential for mammalian brain function. Understanding this process requires simultaneous functional measurements across the cortex. In order to dissociate direct cortico-cortical interactions from other sources of neuronal correlations, it is furthermore desirable to target cross-areal recordings to neuronal subpopulations that anatomically project between areas. Here, we combined anatomical tracers with a novel multi-area two-photon microscope to perform simultaneous calcium imaging across mouse primary (S1) and secondary (S2) somatosensory whisker cortex during texture discrimination behavior, specifically identifying feedforward and feedback neurons. We find that coordination of S1-S2 activity increases during motor behaviors such as goal-directed whisking and licking. This effect was not specific to identified feedforward and feedback neurons. However, these mutually projecting neurons especially participated in inter-areal coordination when motor behavior was paired with whisker-texture touches, suggesting that direct S1-S2 interactions are sensory-dependent. Our results demonstrate specific functional coordination of anatomically-identified projection neurons across sensory cortices.

          DOI: http://dx.doi.org/10.7554/eLife.14679.001

          eLife digest

          Behavior and cognition – the process of thought – emerge from computations that occur within vast networks of neurons in the brain. Within these networks, neurons may communicate with their neighbours in the same brain region as well as with distant counterparts in remote brain regions. Neuroscientists have studied these networks by measuring the activity of neurons within a single region or across the brain as a whole. However, it has not been possible to study long-distance communication between pairs of neurons in different brain regions. This has made it difficult to work out exactly what information brain regions exchange.

          Chen, Voigt et al. now overcome these challenges by developing a new microscope system that allows researchers to measure the activity of individual neurons in different brain regions at the same time. The system works alongside tracing techniques that map the connections between distant neurons.

          To demonstrate the new tools, Chen, Voigt et al. measured the activity of neurons in two areas of the mouse brain that monitor the whiskers. Mice brush their whiskers against an object to obtain information on its size, shape, texture and location. Two brain regions, called the primary and secondary areas of the whisker cortex, process this information and exchange messages back and forth. However, it was unclear what information these messages contain.

          Chen, Voigt et al. therefore trained mice to discriminate between coarse and fine sandpapers using their whiskers, and analysed the activity of the neurons that directly connect the two areas of the whisker cortex. The results revealed that although movement and sensory stimulation activated both the primary and secondary areas of the whisker cortex, the direct connections between these regions mainly exchange sensory information.

          This approach makes it possible to observe brain networks in an unprecedented level of detail. In the future, this technology will be extended to provide a more comprehensive view of how neurons communicate across brain areas. This will increase our understanding of how multiple areas of the brain all work together to produce the activity patterns that give rise to behavior.

          DOI: http://dx.doi.org/10.7554/eLife.14679.002

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          Most cited references53

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          A mesoscale connectome of the mouse brain.

          Comprehensive knowledge of the brain's wiring diagram is fundamental for understanding how the nervous system processes information at both local and global scales. However, with the singular exception of the C. elegans microscale connectome, there are no complete connectivity data sets in other species. Here we report a brain-wide, cellular-level, mesoscale connectome for the mouse. The Allen Mouse Brain Connectivity Atlas uses enhanced green fluorescent protein (EGFP)-expressing adeno-associated viral vectors to trace axonal projections from defined regions and cell types, and high-throughput serial two-photon tomography to image the EGFP-labelled axons throughout the brain. This systematic and standardized approach allows spatial registration of individual experiments into a common three dimensional (3D) reference space, resulting in a whole-brain connectivity matrix. A computational model yields insights into connectional strength distribution, symmetry and other network properties. Virtual tractography illustrates 3D topography among interconnected regions. Cortico-thalamic pathway analysis demonstrates segregation and integration of parallel pathways. The Allen Mouse Brain Connectivity Atlas is a freely available, foundational resource for structural and functional investigations into the neural circuits that support behavioural and cognitive processes in health and disease.
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            Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance.

            An increasingly powerful approach for studying brain circuits relies on targeting genetically encoded sensors and effectors to specific cell types. However, current approaches for this are still limited in functionality and specificity. Here we utilize several intersectional strategies to generate multiple transgenic mouse lines expressing high levels of novel genetic tools with high specificity. We developed driver and double reporter mouse lines and viral vectors using the Cre/Flp and Cre/Dre double recombinase systems and established a new, retargetable genomic locus, TIGRE, which allowed the generation of a large set of Cre/tTA-dependent reporter lines expressing fluorescent proteins, genetically encoded calcium, voltage, or glutamate indicators, and optogenetic effectors, all at substantially higher levels than before. High functionality was shown in example mouse lines for GCaMP6, YCX2.60, VSFP Butterfly 1.2, and Jaws. These novel transgenic lines greatly expand the ability to monitor and manipulate neuronal activities with increased specificity.
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              Top-down influences on visual processing.

              Re-entrant or feedback pathways between cortical areas carry rich and varied information about behavioural context, including attention, expectation, perceptual tasks, working memory and motor commands. Neurons receiving such inputs effectively function as adaptive processors that are able to assume different functional states according to the task being executed. Recent data suggest that the selection of particular inputs, representing different components of an association field, enable neurons to take on different functional roles. In this Review, we discuss the various top-down influences exerted on the visual cortical pathways and highlight the dynamic nature of the receptive field, which allows neurons to carry information that is relevant to the current perceptual demands.

                Author and article information

                Role: Reviewing editor
                eLife Sciences Publications, Ltd
                24 May 2016
                : 5
                : e14679
                [1 ]deptBrain Research Institute , University of Zurich , Zurich, Switzerland
                [2 ]deptNeuroscience Center Zurich , University of Zurich, ETH Zurich , Zurich, Switzerland
                [3]University of Oxford , United Kingdom
                [4]University of Oxford , United Kingdom
                Author notes

                Department of Biology, Boston University, Boston, United States.


                Federal Ministry of Education and Research, Bonn, Germany.


                These authors contributed equally to this work.

                Author information
                © 2016, Chen et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                : 25 January 2016
                : 21 May 2016
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 310030-127091
                Award Recipient :
                Funded by: Swiss SystemsX.ch Initiative;
                Award ID: 2008/2011-Neurochoice
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: BRAIN Initiative 1U01NS090475-01
                Award Recipient :
                Funded by: University of Zurich;
                Award ID: Forschungskredit grant 541541808
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: International Research Fellowship grant 1158914
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Research Article
                Custom metadata
                A new microscopy system allows the activity of interconnected neurons in different brain regions to be measured simultaneously.

                Life sciences
                Life sciences
                two-photon, calcium, whisker, cortex, mouse


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