Spatial encoding in the visual pathway arises in cortex and depends on active navigation

During navigation, responses in primary visual cortex (V1) are modulated by the animal’s position. Here, we show that this modulation is present across multiple higher visual cortical areas but largely absent in geniculate inputs to V1. Spatial modulation is stronger during active navigation than during passive viewing. Moreover, navigation activates different neurons than classical drifting gratings, and promotes the reliability of neural responses in parietal and medial cortical areas.

[1]  Morgane M. Roth,et al.  Distinct Functional Properties of Primary and Posteromedial Visual Area of Mouse Neocortex , 2012, The Journal of Neuroscience.

[2]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[3]  Elina A K Jacobs,et al.  Aberrant Cortical Activity in Multiple GCaMP6-Expressing Transgenic Mouse Lines , 2017, eNeuro.

[4]  A. Grinvald,et al.  A tandem-lens epifluorescence macroscope: Hundred-fold brightness advantage for wide-field imaging , 1991, Journal of Neuroscience Methods.

[5]  Johannes C. Dahmen,et al.  Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex , 2015, Nature Neuroscience.

[6]  M. Carandini,et al.  Mouse Visual Cortex Is Modulated by Distance Traveled and by Theta Oscillations , 2020, Current Biology.

[7]  D. Tank,et al.  Neural Correlates of Cognition in Primary Visual versus Neighboring Posterior Cortices during Visual Evidence-Accumulation-based Navigation , 2019, bioRxiv.

[8]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Lai-Sang Young,et al.  Orientation Selectivity from Very Sparse LGN Inputs in a Comprehensive Model of Macaque V1 Cortex , 2016, The Journal of Neuroscience.

[10]  Y. Dan,et al.  Long-range and local circuits for top-down modulation of visual cortex processing , 2014, Science.

[11]  Matteo Carandini,et al.  Kilosort: realtime spike-sorting for extracellular electrophysiology with hundreds of channels , 2016, bioRxiv.

[12]  Bruno Poucet,et al.  A spatial code in the dorsal lateral geniculate nucleus , 2018, bioRxiv.

[13]  Matteo Carandini,et al.  Cascaded Effects of Spatial Adaptation in the Early Visual System , 2014, Neuron.

[14]  Young Ho Kim,et al.  Role of active movement in place‐specific firing of hippocampal neurons , 2005, Hippocampus.

[15]  Karoline Hovde,et al.  Architecture and organization of mouse posterior parietal cortex relative to extrastriate areas , 2019, The European journal of neuroscience.

[16]  Bruce L. McNaughton,et al.  Sparse orthogonal population representation of spatial context in the retrosplenial cortex , 2017, Nature Communications.

[17]  Bruce L. McNaughton,et al.  Hippocampus-dependent emergence of spatial sequence coding in retrosplenial cortex , 2018, Proceedings of the National Academy of Sciences.

[18]  John A. King,et al.  How vision and movement combine in the hippocampal place code , 2012, Proceedings of the National Academy of Sciences.

[19]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[20]  David J Heeger,et al.  Rapid and precise retinotopic mapping of the visual cortex obtained by voltage-sensitive dye imaging in the behaving monkey. , 2007, Journal of neurophysiology.

[21]  Olaf Sporns,et al.  Network Analysis of Corticocortical Connections Reveals Ventral and Dorsal Processing Streams in Mouse Visual Cortex , 2012, The Journal of Neuroscience.

[22]  Kenneth D. Harris,et al.  Coherent encoding of subjective spatial position in visual cortex and hippocampus , 2018, Nature.

[23]  Kenichi Ohki,et al.  Functional Segregation and Development of Mouse Higher Visual Areas , 2017, The Journal of Neuroscience.

[24]  Tatsuo K Sato,et al.  Imaging the Awake Visual Cortex with a Genetically Encoded Voltage Indicator , 2015, The Journal of Neuroscience.

[25]  Demetris K. Roumis,et al.  Functional Specialization of Mouse Higher Visual Cortical Areas , 2011, Neuron.

[26]  Nathan C. Klapoetke,et al.  Transgenic Mice for Intersectional Targeting of Neural Sensors and Effectors with High Specificity and Performance , 2015, Neuron.

[27]  Bruno Poucet,et al.  Role of the parietal cortex in long-term representation of spatial information in the rat , 2009, Neurobiology of Learning and Memory.

[28]  C. Harvey,et al.  The Spatial Structure of Neural Encoding in Mouse Posterior Cortex during Navigation , 2019, Neuron.

[29]  Quanxin Wang,et al.  Area map of mouse visual cortex , 2007, The Journal of comparative neurology.

[30]  Douglas A Nitz,et al.  Spaces within spaces: rat parietal cortex neurons register position across three reference frames , 2012, Nature Neuroscience.

[31]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[32]  Yun Wang,et al.  Hierarchical organization of cortical and thalamic connectivity , 2019, Nature.

[33]  B. J. Clark,et al.  Interaction of Egocentric and World-Centered Reference Frames in the Rat Posterior Parietal Cortex , 2014, The Journal of Neuroscience.

[34]  E. J. Green,et al.  Cortical representation of motion during unrestrained spatial navigation in the rat. , 1994, Cerebral cortex.

[35]  Lukas F Fischer,et al.  Author response: Representation of visual landmarks in retrosplenial cortex , 2020 .

[36]  Hassana K. Oyibo,et al.  Experience-dependent spatial expectations in mouse visual cortex , 2016, Nature Neuroscience.

[37]  Matteo Carandini,et al.  A tool for analyzing electrode tracks from slice histology , 2018, bioRxiv.

[38]  Hongtu Zhu,et al.  Stream-dependent development of higher visual cortical areas , 2016, Nature Neuroscience.

[39]  Yang Li,et al.  An extended retinotopic map of mouse cortex , 2017, eLife.

[40]  B. Connors,et al.  Differential Regulation of Neocortical Synapses by Neuromodulators and Activity , 1997, Neuron.

[41]  Kenneth D. Harris,et al.  Author response: Decision and navigation in mouse parietal cortex , 2018 .

[42]  Christof Koch,et al.  A large-scale, standardized physiological survey reveals higher order coding throughout the mouse visual cortex , 2018, bioRxiv.

[43]  David K Bilkey,et al.  Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. , 2006, Journal of neurophysiology.

[44]  Takaki Komiyama,et al.  Learning enhances the relative impact of top-down processing in the visual cortex , 2015, Nature Neuroscience.

[45]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[46]  Denise M. Piscopo,et al.  Large-scale imaging of cortical dynamics during sensory perception and behavior. , 2016, Journal of neurophysiology.

[47]  Georg B. Keller,et al.  A Sensorimotor Circuit in Mouse Cortex for Visual Flow Predictions , 2017, Neuron.

[48]  K. Doya,et al.  Neural substrate of dynamic Bayesian inference in the cerebral cortex , 2016, Nature Neuroscience.

[49]  Reiko Meguro,et al.  The Extrageniculate Visual Pathway Generates Distinct Response Properties in the Higher Visual Areas of Mice , 2014, Current Biology.

[50]  Matteo Carandini,et al.  Retinal outputs depend on behavioural state , 2019, bioRxiv.

[51]  L. Frank,et al.  Behavioral/Systems/Cognitive Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments , 2022 .

[52]  M. Häusser,et al.  Cellular mechanisms of spatial navigation in the medial entorhinal cortex , 2013, Nature Neuroscience.

[53]  Edward M. Callaway,et al.  A dedicated circuit linking direction selective retinal ganglion cells to primary visual cortex , 2014, Nature.

[54]  Ovidiu F. Jurjuţ,et al.  Effects of Locomotion Extend throughout the Mouse Early Visual System , 2014, Current Biology.

[55]  David S. Lorberbaum,et al.  Genetic evidence that Nkx2.2 acts primarily downstream of Neurog3 in pancreatic endocrine lineage development , 2017, eLife.

[56]  Ian Nauhaus,et al.  Topography and Areal Organization of Mouse Visual Cortex , 2014, The Journal of Neuroscience.

[57]  M. Carandini,et al.  Integration of visual motion and locomotion in mouse visual cortex , 2013, Nature Neuroscience.

[58]  D. Nitz Tracking Route Progression in the Posterior Parietal Cortex , 2006, Neuron.

[59]  Daoyun Ji,et al.  Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior , 2015, eLife.

[60]  Mattias P. Karlsson,et al.  Network Dynamics Underlying the Formation of Sparse, Informative Representations in the Hippocampus , 2008, The Journal of Neuroscience.

[61]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[62]  J. O’Keefe,et al.  Grid cell firing patterns signal environmental novelty by expansion , 2012, Proceedings of the National Academy of Sciences.

[63]  Mario Dipoppa,et al.  Suite2p: beyond 10,000 neurons with standard two-photon microscopy , 2016, bioRxiv.

[64]  Daoyun Ji,et al.  Author response: Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior , 2015 .

[65]  B. McNaughton,et al.  Self-Motion and the Hippocampal Spatial Metric , 2005, The Journal of Neuroscience.

[66]  James H. Marshel,et al.  Functional Specialization of Seven Mouse Visual Cortical Areas , 2011, Neuron.

[67]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[68]  Kenneth D Harris,et al.  Decision and navigation in mouse parietal cortex , 2017, bioRxiv.

[69]  Gerit Pfuhl,et al.  Functional Split between Parietal and Entorhinal Cortices in the Rat , 2012, Neuron.