Coherent encoding of subjective spatial position in visual cortex and hippocampus

A major role of vision is to guide navigation, and navigation is strongly driven by vision 1 – 4 . 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 the visual cortex 6 , 7...

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Published in:	Nature (London) Vol. 562; no. 7725; pp. 124 - 127
Main Authors:	Saleem, Aman B., Diamanti, E. Mika, Fournier, Julien, Harris, Kenneth D., Carandini, Matteo
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 01.10.2018 Nature Publishing Group
Subjects:	14/69 631/378/116 631/378/1595/3922 631/378/2613 631/378/3917 631/378/3920 64/110 64/60 Animals Brain Brain research Coding Computer applications Female Hippocampus Hippocampus (Brain) Hippocampus - cytology Hippocampus - physiology Humanities and Social Sciences Information processing Landmarks Letter Life Sciences Male Mice Mice, Inbred C57BL Modulation multidisciplinary Navigation Navigation behavior Neurons Neurons - physiology Neurons and Cognition Populations Reinforcement Representations Reward Science Science (multidisciplinary) Sensory integration Somatosensory cortex Space perception Spatial Behavior - physiology Spatial Processing - physiology Virtual Reality Visual cortex Visual Cortex - cytology Visual Cortex - physiology Visual signals Reward Zone Reward Regions Pupil Position Water Reward Running Speed
ISSN:	0028-0836, 1476-4687, 1476-4687
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Abstract	A major role of vision is to guide navigation, and navigation is strongly driven by vision 1 – 4 . 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 the visual cortex 6 , 7 . Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location—whether correctly or incorrectly—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 a primary sensory area suggests that they permeate sensory processing in the cortex. When running through a virtual reality corridor, a mouse’s position is represented in both the hippocampus (as expected) and the primary visual cortex, for places that are visually identical.
AbstractList	A major role of vision is to guide navigation, and navigation is strongly driven by vision1-4. Indeed, the brain's visual and navigational systems are known to interact5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location-whether correctly or incorrectly-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 a primary sensory area suggests that they permeate sensory processing in the cortex.A major role of vision is to guide navigation, and navigation is strongly driven by vision1-4. Indeed, the brain's visual and navigational systems are known to interact5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location-whether correctly or incorrectly-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 a primary sensory area suggests that they permeate sensory processing in the cortex. A major role of vision is to guide navigation, and navigation is strongly driven by vision.sup.1-4. Indeed, the brain's visual and navigational systems are known to interact.sup.5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex.sup.6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location--whether correctly or incorrectly--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 a primary sensory area suggests that they permeate sensory processing in the cortex. A major role of vision is to guide navigation, and navigation is strongly driven by vision1–4. Indeed, the brain’s visual and navigational systems are known to interact5,6, and signals related to position in the environment have been suggested to appear as early as in visual cortex6,7. 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. A major role of vision is to guide navigation, and navigation is strongly driven by vision 1 – 4 . 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 the visual cortex 6 , 7 . Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location—whether correctly or incorrectly—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 a primary sensory area suggests that they permeate sensory processing in the cortex. When running through a virtual reality corridor, a mouse’s position is represented in both the hippocampus (as expected) and the primary visual cortex, for places that are visually identical. A major role of vision is to guide navigation, and navigation is strongly driven by vision . Indeed, the brain's visual and navigational systems are known to interact , and signals related to position in the environment have been suggested to appear as early as in the visual cortex . Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location-whether correctly or incorrectly-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 a primary sensory area suggests that they permeate sensory processing in the cortex. A major role of vision is to guide navigation, and navigation is strongly driven by vision.sup.1-4. Indeed, the brain's visual and navigational systems are known to interact.sup.5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex.sup.6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location--whether correctly or incorrectly--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 a primary sensory area suggests that they permeate sensory processing in the cortex.When running through a virtual reality corridor, a mouse's position is represented in both the hippocampus (as expected) and the primary visual cortex, for places that are visually identical. A major role of vision is to guide navigation, and navigation is strongly driven by vision1-4. Indeed, the brain's visual and navigational systems are known to interact5,6, and signals related to position in the environment have been suggested to appear as early as in the visual cortex6,7. Here, to establish the nature of these signals, we recorded in the primary visual cortex (V1) and 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 at those positions. Most V1 neurons, however, responded solely or more strongly to the landmarks in one position rather than the other. 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. When animals licked in a given location-whether correctly or incorrectly-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 a primary sensory area suggests that they permeate sensory processing in the cortex.
Audience	Academic
Author	Saleem, Aman B. Fournier, Julien Harris, Kenneth D. Carandini, Matteo Diamanti, E. Mika
AuthorAffiliation	4 UCL Institute of Neurology, University College London, London, WC1N 3BG, UK 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
AuthorAffiliation_xml	– name: 3 CoMPLEX, Department of Computer Science, University College London, London, WC1E 6BT, UK – name: 1 UCL Institute of Ophthalmology, University College London, London, EC1V9EL, UK – name: 2 Department of Experimental Psychology, University College London, London, WC1H 0AP, UK – name: 4 UCL Institute of Neurology, University College London, London, WC1N 3BG, UK
Author_xml	– sequence: 1 givenname: Aman B. surname: Saleem fullname: Saleem, Aman B. email: aman.saleem@ucl.ac.uk organization: UCL Institute of Ophthalmology, University College London, Department of Experimental Psychology, University College London – sequence: 2 givenname: E. Mika surname: Diamanti fullname: Diamanti, E. Mika organization: UCL Institute of Ophthalmology, University College London, CoMPLEX, Department of Computer Science, University College London – sequence: 3 givenname: Julien surname: Fournier fullname: Fournier, Julien organization: UCL Institute of Ophthalmology, University College London – sequence: 4 givenname: Kenneth D. surname: Harris fullname: Harris, Kenneth D. organization: UCL Institute of Neurology, University College London – sequence: 5 givenname: Matteo surname: Carandini fullname: Carandini, Matteo organization: UCL Institute of Ophthalmology, University College London
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/30202092$$D View this record in MEDLINE/PubMed https://hal.science/hal-03949451$$DView record in HAL
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ContentType	Journal Article
Copyright	Springer Nature Limited 2018 COPYRIGHT 2018 Nature Publishing Group Copyright Nature Publishing Group Oct 4, 2018 Distributed under a Creative Commons Attribution 4.0 International License
Copyright_xml	– notice: Springer Nature Limited 2018 – notice: COPYRIGHT 2018 Nature Publishing Group – notice: Copyright Nature Publishing Group Oct 4, 2018 – notice: Distributed under a Creative Commons Attribution 4.0 International License
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DOI	10.1038/s41586-018-0516-1
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Keywords	Reward Zone Reward Regions Pupil Position Water Reward Running Speed
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Title	Coherent encoding of subjective spatial position in visual cortex and hippocampus
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