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      Decision and navigation in mouse parietal cortex

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          Abstract

          Posterior parietal cortex (PPC) has been implicated in navigation, in the control of movement, and in visually-guided decisions. To relate these views, we measured activity in PPC while mice performed a virtual navigation task driven by visual decisions. PPC neurons were selective for specific combinations of the animal's spatial position and heading angle. This selectivity closely predicted both the activity of individual PPC neurons, and the arrangement of their collective firing patterns in choice-selective sequences. These sequences reflected PPC encoding of the animal’s navigation trajectory. Using decision as a predictor instead of heading yielded worse fits, and using it in addition to heading only slightly improved the fits. Alternative models based on visual or motor variables were inferior. We conclude that when mice use vision to choose their trajectories, a large fraction of parietal cortex activity can be predicted from simple attributes such as spatial position and heading.

          eLife digest

          When we step out of our homes in the morning, we scan our surroundings to decide which path we should take. It is still unclear whether we use different brain areas to examine the environment, decide on a route, and then set our trajectory, or if a single region can play a role in all three processes. An area in the top of our brain, named the posterior parietal cortex (PPC), may be an intriguing candidate: some studies find that this region is involved in vision, others highlight that it takes part in decision-making, and a third group of experiments shows that it is important for setting paths. Could the PPC be integrating all three types of information, or might the activity of the neurons in this area be better explained by just one of these processes?

          Here, Krumin et al. trained mice to use visual clues to navigate a virtual reality maze, where they have to ‘walk’ down a corridor and then choose to ‘go down’ the right or the left arm. The rodents move on a ball suspended in mid-air, which acts as a treadmill. Meanwhile, the head of the animal is kept still, making it easier to image the activity of hundreds of neurons in the PPC.

          The experiments show that when the mouse uses its vision to choose its trajectory, the PPC does not encode visual signals or abstract decisions. Instead, two navigational attributes – the position of the animal along the corridor and its heading angle – activate neurons in this area. Knowing these two features was enough for Krumin et al. to accurately predict the activity of the neurons in the PPC.

          This means that we can forecast the activity of neurons deep in the brain by recording simple behavioral features. The results also suggest that the PPC may be more important for setting trajectories than for processing visual images or making abstract decisions. If these findings were to be confirmed in humans, where the parietal cortex is much more complex, they might help understand better the problems that arise when this area is damaged, for example after a stroke.

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          Most cited references41

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          The importance of mixed selectivity in complex cognitive tasks.

          Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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            Choice-specific sequences in parietal cortex during a virtual-navigation decision task

            The posterior parietal cortex (PPC) plays an important role in many cognitive behaviors; however, the neural circuit dynamics underlying PPC function are not well understood. Here we optically imaged the spatial and temporal activity patterns of neuronal populations in mice performing a PPC-dependent task that combined a perceptual decision and memory-guided navigation in a virtual environment. Individual neurons had transient activation staggered relative to one another in time, forming a sequence of neuronal activation spanning the entire length of a task trial. Distinct sequences of neurons were triggered on trials with opposite behavioral choices and defined divergent, choice-specific trajectories through a state space of neuronal population activity. Cells participating in the different sequences and at distinct time points in the task were anatomically intermixed over microcircuit length scales (< 100 micrometers). During working memory decision tasks the PPC may therefore perform computations through sequence-based circuit dynamics, rather than long-lived stable states, implemented using anatomically intermingled microcircuits.
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              Neural correlates of decision variables in parietal cortex.

              Decision theory proposes that humans and animals decide what to do in a given situation by assessing the relative value of each possible response. This assessment can be computed, in part, from the probability that each action will result in a gain and the magnitude of the gain expected. Here we show that the gain (or reward) a monkey can expect to realize from an eye-movement response modulates the activity of neurons in the lateral intraparietal area, an area of primate cortex that is thought to transform visual signals into eye-movement commands. We also show that the activity of these neurons is sensitive to the probability that a particular response will result in a gain. When animals can choose freely between two alternative responses, the choices subjects make and neuronal activation in this area are both correlated with the relative amount of gain that the animal can expect from each response. Our data indicate that a decision-theoretic model may provide a powerful new framework for studying the neural processes that intervene between sensation and action.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                23 November 2018
                2018
                : 7
                : e42583
                Affiliations
                [1 ]deptUCL Institute of Ophthalmology University College London LondonUnited Kingdom
                [2 ]deptUCL Institute of Neurology University College London LondonUnited Kingdom
                University of Pennsylvania United States
                University of Pennsylvania United States
                University of Pennsylvania United States
                Author information
                http://orcid.org/0000-0001-7356-6994
                http://orcid.org/0000-0002-7293-8538
                http://orcid.org/0000-0002-5930-6456
                http://orcid.org/0000-0003-4880-7682
                Article
                42583
                10.7554/eLife.42583
                6300355
                30468146
                aabbc4f0-5594-4101-a66e-49e5c1018145
                © 2018, Krumin 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.

                History
                : 04 October 2018
                : 16 November 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 109004
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: 325512
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 095668
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 205093
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 108726
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 095669
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: CORTEX
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                When mice use vision to choose their trajectories, a large fraction of parietal cortex activity can be precisely predicted from navigational attributes such as spatial position and heading.

                Life sciences
                cortex,navigation,decision,visual processing,mouse
                Life sciences
                cortex, navigation, decision, visual processing, mouse

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