Distinct higher-order thalamic circuits channel parallel streams of visual information in mice

Higher-order thalamic nuclei, such as the visual pulvinar, play essential roles in shaping cortical dynamics and connecting functionally-related cortical and subcortical brain regions. A coherent framework describing pulvinar function remains elusive due to its anatomical complexity, involvement in diverse cognitive processes, and the limited experimental tools available in many species. We combined large-scale anatomical circuit mapping with high-density electrophysiological recordings to dissect a homolog of pulvinar in mice, the lateral posterior nucleus (LP). We define three LP subregions based on correspondence between connectivity and functional properties. These subregions form parallel corticothalamic loops and contain separate representations of visual space. Silencing visual cortex or the superior colliculus revealed that these input sources drive activity and shape visual tuning in separate LP subregions. By specifying the information carried by distinct circuits through LP and identifying their downstream targets, our data provide a roadmap for understanding pulvinar function in visual processing and behavior.

[1]  Edward M. Callaway,et al.  A Disynaptic Relay from Superior Colliculus to Dorsal Stream Visual Cortex in Macaque Monkey , 2010, Neuron.

[2]  Vivien A. Casagrande,et al.  Gating and control of primary visual cortex by pulvinar , 2012, Nature Neuroscience.

[3]  Terry T. Takahashi,et al.  The organization of the lateral thalamus of the hooded rat , 1985, The Journal of comparative neurology.

[4]  B. Frost,et al.  Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons , 1998, Nature Neuroscience.

[5]  H. Hioki,et al.  Different cortical projections from three subdivisions of the rat lateral posterior thalamic nucleus: a single‐neuron tracing study with viral vectors , 2015, The European journal of neuroscience.

[6]  S. Petersen,et al.  Contributions of the pulvinar to visual spatial attention , 1987, Neuropsychologia.

[7]  Samuel D. Gale,et al.  Distinct Representation and Distribution of Visual Information by Specific Cell Types in Mouse Superficial Superior Colliculus , 2014, The Journal of Neuroscience.

[8]  Y. Saalmann,et al.  Cognitive and Perceptual Functions of the Visual Thalamus , 2011, Neuron.

[9]  R. Rafal,et al.  Deficits in spatial coding and feature binding following damage to spatiotopic maps in the human pulvinar , 2002, Nature Neuroscience.

[10]  S. Molotchnikoff,et al.  Influence of the superior colliculus on visual responses of cells in the rabbit's lateral posterior nucleus , 2004, Experimental Brain Research.

[11]  Annette E. Allen,et al.  Visual input to the mouse lateral posterior and posterior thalamic nuclei: photoreceptive origins and retinotopic order , 2016, The Journal of physiology.

[12]  M. Bickford,et al.  Ultrastructural examination of diffuse and specific tectopulvinar projections in the tree shrew , 2008, The Journal of comparative neurology.

[13]  Lydia Ng,et al.  The organization of intracortical connections by layer and cell class in the mouse brain , 2018, bioRxiv.

[14]  Glyn W. Humphreys,et al.  Impaired attentional selection following lesions to human pulvinar: Evidence for homology between human and monkey , 2009, Proceedings of the National Academy of Sciences.

[15]  Jumpei Matsumoto,et al.  Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes , 2013, Proceedings of the National Academy of Sciences.

[16]  Allan R. Jones,et al.  A mesoscale connectome of the mouse brain , 2014, Nature.

[17]  M. Bickford,et al.  The mouse pulvinar nucleus: Organization of the tectorecipient zones , 2017, Visual Neuroscience.

[18]  Robert Desimone,et al.  Pulvinar-Cortex Interactions in Vision and Attention , 2016, Neuron.

[19]  Zengcai V. Guo,et al.  Flow of Cortical Activity Underlying a Tactile Decision in Mice , 2014, Neuron.

[20]  Robert H. Wurtz,et al.  Signals Conveyed in the Pulvinar Pathway from Superior Colliculus to Cortical Area MT , 2011, The Journal of Neuroscience.

[21]  S Murray Sherman,et al.  Thalamus plays a central role in ongoing cortical functioning , 2016, Nature Neuroscience.

[22]  R. Wurtz,et al.  A circuit for saccadic suppression in the primate brain. , 2017, Journal of neurophysiology.

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

[24]  G. Laurent,et al.  Computation of Object Approach by a Wide-Field, Motion-Sensitive Neuron , 1999, The Journal of Neuroscience.

[25]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

[26]  C. Gerfen,et al.  GENSAT BAC Cre-Recombinase Driver Lines to Study the Functional Organization of Cerebral Cortical and Basal Ganglia Circuits , 2013, Neuron.

[27]  G. Feng,et al.  Cell type–specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function , 2011, Nature Methods.

[28]  Stefan Mihalas,et al.  A Comparison of Visual Response Properties in the Lateral Geniculate Nucleus and Primary Visual Cortex of Awake and Anesthetized Mice , 2016, The Journal of Neuroscience.

[29]  P. Moran.  Notes on continuous stochastic phenomena. , 1950, Biometrika.

[30]  Sabine Kastner,et al.  Thalamic functions in distributed cognitive control , 2017, Nature Neuroscience.

[31]  D. B. Bender.  Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus , 1983, Brain Research.

[32]  Jon H. Kaas,et al.  Pulvinar contributions to the dorsal and ventral streams of visual processing in primates , 2007, Brain Research Reviews.

[33]  Mehran Ahmadlou,et al.  Preference for concentric orientations in the mouse superior colliculus , 2015, Nature Communications.

[34]  Rebecca A. Mease,et al.  Convergence of Cortical and Sensory Driver Inputs on Single Thalamocortical Cells , 2013, Cerebral cortex.

[35]  Yang Li,et al.  Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice , 2018, Nature Communications.

[36]  Zengcai V. Guo,et al.  Maintenance of persistent activity in a frontal thalamocortical loop , 2017, Nature.

[37]  Jon H Kaas,et al.  Projections of the superior colliculus to the pulvinar in prosimian galagos (Otolemur garnettii) and VGLUT2 staining of the visual pulvinar , 2013, The Journal of comparative neurology.

[38]  Shay Ohayon,et al.  Open Ephys: an open-source, plugin-based platform for multichannel electrophysiology , 2017, Journal of neural engineering.

[39]  Allan R. Jones,et al.  A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing , 2012, Nature Neuroscience.

[40]  Saskia E. J. de Vries,et al.  Loom-Sensitive Neurons Link Computation to Action in the Drosophila Visual System , 2012, Current Biology.

[41]  Bert Sakmann,et al.  Cortical Dependence of Whisker Responses in Posterior Medial Thalamus In Vivo , 2016, Cerebral cortex.

[42]  Cyrille Rossant,et al.  Spike sorting for large, dense electrode arrays , 2015 .

[43]  Xintian Hu,et al.  Corrigendum: Processing of visually evoked innate fear by a non-canonical thalamic pathway , 2015, Nature Communications.

[44]  S Shipp,et al.  The functional logic of cortico-pulvinar connections. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[45]  Samuel D. Gale,et al.  Active Dendritic Properties and Local Inhibitory Input Enable Selectivity for Object Motion in Mouse Superior Colliculus Neurons , 2016, The Journal of Neuroscience.

[46]  D. Hubel,et al.  Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. , 1975, Journal of neurophysiology.

[47]  Yong-Jun Liu,et al.  Neuronal Responses to Looming Objects in the Superior Colliculus of the Cat , 2011, Brain, Behavior and Evolution.

[48]  Jamie L. Reed,et al.  Superior colliculus connections with visual thalamus in gray squirrels (Sciurus carolinensis): Evidence for four subdivisions within the pulvinar complex , 2011, The Journal of comparative neurology.

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

[50]  Jianhua Cang,et al.  Visual Cortex Modulates the Magnitude but Not the Selectivity of Looming-Evoked Responses in the Superior Colliculus of Awake Mice , 2014, Neuron.

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

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

[53]  Quanxin Wang,et al.  Stream-Related Preferences of Inputs to the Superior Colliculus from Areas of Dorsal and Ventral Streams of Mouse Visual Cortex , 2013, The Journal of Neuroscience.

[54]  A. Butler.  Evolution of the thalamus: a morphological and functional review , 2008 .

[55]  P. Cavanagh,et al.  Deep tectal cells in pigeons respond to kinematograms , 1988, Journal of Comparative Physiology A.

[56]  Kenneth D. Harris,et al.  Fast and accurate spike sorting of high-channel count probes with KiloSort , 2016, NIPS.

[57]  Ralf D. Wimmer,et al.  Thalamic amplification of cortical connectivity sustains attentional control , 2017, Nature.

[58]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[59]  Samuel D. Gale,et al.  Distinct cell types in the superficial superior colliculus project to the dorsal lateral geniculate and lateral posterior thalamic nuclei , 2018, Journal of neurophysiology.

[60]  Ian R. Wickersham,et al.  Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons , 2007, Neuron.

[61]  R. Wurtz,et al.  Functional Identification of a Pulvinar Path from Superior Colliculus to Cortical Area MT , 2010, The Journal of Neuroscience.

[62]  Jon H Kaas,et al.  The evolution and functions of nuclei of the visual pulvinar in primates , 2017, The Journal of comparative neurology.

[63]  Paul G Anastasiades,et al.  Reciprocal Circuits Linking the Prefrontal Cortex with Dorsal and Ventral Thalamic Nuclei , 2018, Neuron.

[64]  Sergey L. Gratiy,et al.  Fully integrated silicon probes for high-density recording of neural activity , 2017, Nature.

[65]  D. Hubel,et al.  Topography of visual and somatosensory projections to mouse superior colliculus. , 1976, Journal of neurophysiology.

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