Distinct organization of two cortico-cortical feedback pathways

Neocortical feedback is critical for processes like attention, prediction, and learning. A mechanistic understanding of its function requires deciphering its cell-type wiring logic. Recent studies revealed a disinhibitory circuit between motor and sensory areas in mice, where feedback preferentially targets vasointestinal peptide-expressing interneurons, in addition to pyramidal cells. It is unknown whether this circuit motif is a general cortico-cortical feedback organizing principle. Combining multiple simultaneous whole-cell recordings with optogenetics we found that in contrast to this wiring rule, feedback between the hierarchically organized visual areas (lateral-medial to V1) preferentially activated somatostatin-expressing interneurons. Functionally, both feedback circuits temporally sharpened feed-forward excitation by eliciting a transient increase followed by a prolonged decrease in pyramidal firing rate under sustained feed-forward input. However, under feed-forward transient input, the motor-sensory feedback facilitated pyramidal cell bursting while visual feedback increased spike time precision. Our findings argue for multiple feedback motifs implementing different dynamic non-linear operations.

[1]  R. Tremblay,et al.  Neocortical Somatostatin-Expressing GABAergic Interneurons Disinhibit the Thalamorecipient Layer 4 , 2013, Neuron.

[2]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[3]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[4]  S. Sherman.  Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[5]  H. Swadlow.  Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. , 2003, Cerebral cortex.

[6]  Mark T. Harnett,et al.  Nonlinear dendritic integration of sensory and motor input during an active sensing task , 2012, Nature.

[7]  K. Svoboda,et al.  Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections , 2007, Nature Neuroscience.

[8]  Allan R. Jones,et al.  Shared and distinct transcriptomic cell types across neocortical areas , 2018, Nature.

[9]  Lindsey L. Glickfeld,et al.  A mouse model of higher visual cortical function , 2014, Current Opinion in Neurobiology.

[10]  F C Hoppensteadt,et al.  The searchlight hypothesis , 1991, Journal of mathematical biology.

[11]  C. Gilbert,et al.  Attention Modulates Contextual Influences in the Primary Visual Cortex of Alert Monkeys , 1999, Neuron.

[12]  Massimo Scanziani,et al.  Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex , 2007, Nature Neuroscience.

[13]  A. Burkhalter,et al.  Hierarchical organization of areas in rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Guangying K. Wu,et al.  Lateral Sharpening of Cortical Frequency Tuning by Approximately Balanced Inhibition , 2008, Neuron.

[15]  G. Feng,et al.  Acute brain slice methods for adult and aging animals: application of targeted patch clamp analysis and optogenetics. , 2014, Methods in molecular biology.

[16]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Angelucci,et al.  Top-down feedback controls spatial summation and response amplitude in primate visual cortex , 2018, Nature Communications.

[18]  Christof Koch,et al.  Physiology of Layer 5 Pyramidal Neurons in Mouse Primary Visual Cortex: Coincidence Detection through Bursting , 2015, PLoS Comput. Biol..

[19]  A. Angelucci,et al.  Circuits and Mechanisms for Surround Modulation in Visual Cortex. , 2017, Annual review of neuroscience.

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

[21]  V. Murthy,et al.  Functional Properties of Cortical Feedback Projections to the Olfactory Bulb , 2012, Neuron.

[22]  B. Sakmann,et al.  Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. , 1993, The Journal of physiology.

[23]  Jeannette A. M. Lorteije,et al.  Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1 , 2019, Current Biology.

[24]  Bryan M Hooks,et al.  Distinct Balance of Excitation and Inhibition in an Interareal Feedforward and Feedback Circuit of Mouse Visual Cortex , 2013, The Journal of Neuroscience.

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

[26]  Morgane M. Roth,et al.  A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex , 2020, Neuron.

[27]  Quanxin Wang,et al.  Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas , 2016, eLife.

[28]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

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

[30]  S. Cruikshank,et al.  Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex , 2007, Nature Neuroscience.

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

[32]  S. Sherman,et al.  A modulatory effect of the feedback from higher visual areas to V1 in the mouse. , 2013, Journal of neurophysiology.

[33]  P. Dayan,et al.  A mathematical model explains saturating axon guidance responses to molecular gradients , 2016, eLife.

[34]  M. Frotscher,et al.  Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network , 2001, The Journal of Neuroscience.

[35]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[36]  George H. Denfield,et al.  Pupil Fluctuations Track Fast Switching of Cortical States during Quiet Wakefulness , 2014, Neuron.

[37]  S. Denéve,et al.  Neural processing as causal inference , 2011, Current Opinion in Neurobiology.

[38]  Quanxin Wang,et al.  Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex , 2011, The Journal of Neuroscience.

[39]  M. Larkum.  A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex , 2013, Trends in Neurosciences.

[40]  Alexander S. Ecker,et al.  Principles of connectivity among morphologically defined cell types in adult neocortex , 2015, Science.

[41]  Richard T Born,et al.  Corticocortical Feedback Contributes to Surround Suppression in V1 of the Alert Primate , 2013, The Journal of Neuroscience.

[42]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[43]  Andreas Burkhalter,et al.  Distinct GABAergic Targets of Feedforward and Feedback Connections Between Lower and Higher Areas of Rat Visual Cortex , 2003, The Journal of Neuroscience.

[44]  L. Petreanu,et al.  The functional organization of cortical feedback inputs to primary visual cortex , 2018, Nature Neuroscience.

[45]  S. Manita,et al.  A Top-Down Cortical Circuit for Accurate Sensory Perception , 2015, Neuron.

[46]  G. Fishell,et al.  The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors , 2010, The Journal of Neuroscience.

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

[48]  Ian Nauhaus,et al.  Contrast Dependence and Differential Contributions from Somatostatin- and Parvalbumin-Expressing Neurons to Spatial Integration in Mouse V1 , 2013, The Journal of Neuroscience.

[49]  H. Adesnik,et al.  A neural circuit for spatial summation in visual cortex , 2012, Nature.

[50]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[51]  G. Fishell,et al.  Interneuron cell types are fit to function , 2014, Nature.

[52]  Tai Sing Lee,et al.  Hierarchical Bayesian inference in the visual cortex. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[53]  S. Sherman,et al.  Synaptic Properties of Corticocortical Connections between the Primary and Secondary Visual Cortical Areas in the Mouse , 2011, The Journal of Neuroscience.

[54]  R. Tremblay,et al.  GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits , 2016, Neuron.

[55]  D. Contreras,et al.  Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex , 2005, Nature Neuroscience.

[56]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[57]  Karl J. Friston,et al.  Does predictive coding have a future? , 2018, Nature Neuroscience.

[58]  Ariel Agmon,et al.  Not all that glitters is gold: off-target recombination in the somatostatin–IRES-Cre mouse line labels a subset of fast-spiking interneurons , 2013, Front. Neural Circuits.

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

[60]  Ivan Cohen,et al.  Diversity and overlap of parvalbumin and somatostatin expressing interneurons in mouse presubiculum , 2015, Front. Neural Circuits.

[61]  A. Borst.  Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[62]  Karel Svoboda,et al.  Long-Range Neuronal Circuits Underlying the Interaction between Sensory and Motor Cortex , 2011, Neuron.

[63]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[64]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[65]  H. Markram,et al.  Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells , 2007, Neuron.

[66]  Shane R. Crandall,et al.  A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses , 2015, Neuron.

[67]  Xiaolong Jiang,et al.  The organization of two new cortical interneuronal circuits , 2013, Nature Neuroscience.

[68]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[69]  J. Bullier,et al.  Functional interactions between areas V1 and V2 in the monkey , 1996, Journal of Physiology-Paris.

[70]  Caspar M. Schwiedrzik,et al.  High-Level Prediction Signals in a Low-Level Area of the Macaque Face-Processing Hierarchy , 2017, Neuron.

[71]  Victor A. F. Lamme,et al.  Feedforward, horizontal, and feedback processing in the visual cortex , 1998, Current Opinion in Neurobiology.

[72]  Anders Lansner,et al.  Long-range recruitment of Martinotti cells causes surround suppression and promotes saliency in an attractor network model , 2015, Front. Neural Circuits.

[73]  Farran Briggs,et al.  Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret , 2017, Proceedings of the National Academy of Sciences.

[74]  Li I. Zhang,et al.  Intervening Inhibition Underlies Simple-Cell Receptive Field Structure in Visual Cortex , 2009, Nature Neuroscience.

[75]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

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

[77]  H. Cabral,et al.  Multiple Comparisons Procedures , 2008, Circulation.