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      Coherent encoding of subjective spatial position in visual cortex and hippocampus

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          Abstract

          A major role of vision is to guide navigation, and navigation is strongly driven by vision 14. Indeed, the brain’s visual and navigational systems are known to interact 5, 6, and signals related to position in the environment have been suggested to appear as early as in visual cortex 6, 7. To establish the nature of these signals we recorded in primary visual cortex (V1) and in hippocampal area CA1 while mice traversed a corridor in virtual reality. The corridor contained identical visual landmarks in two positions, so that a purely visual neuron would respond similarly in those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position. This modulation of visual responses by spatial location was not explained by factors such as running speed. To assess whether the modulation is related to navigational signals and to the animal’s subjective estimate of position, we trained the mice to lick for a water reward upon reaching a reward zone in the corridor. Neuronal populations in both CA1 and V1 encoded the animal’s position along the corridor, and the errors in their representations were correlated. Moreover, both representations reflected the animal’s subjective estimate of position, inferred from the animal’s licks, better than its actual position. Indeed, when animals licked in a given location – whether correct or incorrect – neural populations in both V1 and CA1 placed the animal in the reward zone. We conclude that visual responses in V1 are controlled by navigational signals, which are coherent with those encoded in hippocampus and reflect the animal’s subjective position. The presence of such navigational signals as early as in a primary sensory area suggests that they permeate sensory processing in the cortex.

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          Most cited references36

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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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            The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells.

            Using the techniques set out in the preceding paper (Muller et al., 1987), we investigated the response of place cells to changes in the animal's environment. The standard apparatus used was a cylinder, 76 cm in diameter, with walls 51 cm high. The interior was uniformly gray except for a white cue card that ran the full height of the wall and occupied 100 degrees of arc. The floor of the apparatus presented no obstacles to the animal's motions. Each of these major features of the apparatus was varied while the others were held constant. One set of manipulations involved the cue card. Rotating the cue card produced equal rotations of the firing fields of single cells. Changing the width of the card did not affect the size, shape, or radial position of firing fields, although sometimes the field rotated to a modest extent. Removing the cue card altogether also left the size, shape, and radial positions of firing fields unchanged, but caused fields to rotate to unpredictable angular positions. The second set of manipulations dealt with the size and shape of the apparatus wall. When the standard (small) cylinder was scaled up in diameter and height by a factor of 2, the firing fields of 36% of the cells observed in both cylinders also scaled, in the sense that the field stayed at the same angular position and at the same relative radial position. Of the cells recorded in both cylinders, 52% showed very different firing patterns in one cylinder than in the other. The remaining 12% of the cells were virtually silent in both cylinders. Similar results were obtained when individual cells were recorded in both a small and a large rectangular enclosure. By contrast, when the apparatus floor plan was changed from circular to rectangular, the firing pattern of a cell in an apparatus of one shape could not be predicted from a knowledge of the firing pattern in the other shape. The final manipulations involved placing vertical barriers into the otherwise unobstructed floor of the small cylinder. When an opaque barrier was set up to bisect a previously recorded firing field, in almost all cases the firing field was nearly abolished. This was true even though the barrier occupied only a small fraction of the firing field area. A transparent barrier was effective as the opaque barrier in attenuating firing fields. The lead base used to anchor the vertical barriers did not affect place cell firing.(ABSTRACT TRUNCATED AT 400 WORDS)
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              Intracellular dynamics of hippocampal place cells during virtual navigation

              Hippocampal place cells encode spatial information in rate and temporal codes. To examine the mechanisms underlying hippocampal coding, we measured the intracellular dynamics of place cells by combining in vivo whole cell recordings with a virtual reality system. Head-restrained mice, running on a spherical treadmill, interacted with a computer-generated visual environment to perform spatial behaviors. Robust place cell activity was present during movement along a virtual linear track. From whole cell recordings, we identified three subthreshold signatures of place fields: (1) an asymmetric ramp-like depolarization of the baseline membrane potential; (2) an increase in the amplitude of intracellular theta oscillations; and, (3) a phase precession of the intracellular theta oscillation relative to the extracellularly-recorded theta rhythm. These intracellular dynamics underlie the primary features of place cell rate and temporal codes. The virtual reality system developed here will enable new experimental approaches to study the neural circuits underlying navigation.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                18 December 2018
                10 September 2018
                October 2018
                10 March 2019
                : 562
                : 7725
                : 124-127
                Affiliations
                [1 ]UCL Institute of Ophthalmology, University College London, London, EC1V9EL, UK
                [2 ]Department of Experimental Psychology, University College London, London, WC1H 0AP, UK
                [3 ]CoMPLEX, Department of Computer Science, University College London, London, WC1E 6BT, UK
                [4 ]UCL Institute of Neurology, University College London, London, WC1N 3BG, UK
                Author notes
                [*]

                These authors jointly supervised this work.

                Article
                EMS78784
                10.1038/s41586-018-0516-1
                6309439
                30202092
                97569dbc-468e-4a0b-aa7f-878e9d90cb26

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