Cortical synaptic architecture supports flexible sensory computations

Establishing the fundamental principles that underlie the integration of excitatory and inhibitory presynaptic input populations is crucial to understanding how individual cortical neurons transform signals from peripheral receptors. Here we review recent studies using novel tools to examine the functional properties of excitatory synaptic inputs and the tuning of excitation and inhibition onto individual neurons. New evidence challenges existing synaptic connectivity rules and suggests a more complex functional synaptic architecture that supports a broad range of operations, enabling single neurons to encode multiple sensory features and flexibly shape their computations in the face of diverse sensory input.

[1]  Daniel B. Rubin,et al.  The Stabilized Supralinear Network: A Unifying Circuit Motif Underlying Multi-Input Integration in Sensory Cortex , 2015, Neuron.

[2]  Richard Naud,et al.  Classes of dendritic information processing , 2019, Current Opinion in Neurobiology.

[3]  David E. Whitney,et al.  Orientation selectivity and the functional clustering of synaptic inputs in primary visual cortex , 2016, Nature Neuroscience.

[4]  Nathalie L Rochefort,et al.  Functional mapping of single spines in cortical neurons in vivo , 2011, Nature.

[5]  Takashi Kawashima,et al.  A genetically encoded fluorescent sensor for in vivo imaging of GABA , 2018, Nature Methods.

[6]  C. Blakemore,et al.  Effects of bicuculline on functions of inhibition in visual cortex , 1974, Nature.

[7]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[8]  D. Fitzpatrick,et al.  Differential tuning of excitation and inhibition shapes direction selectivity in ferret V1 , 2018, Nature.

[9]  William N. Grimes,et al.  Flexible Neural Hardware Supports Dynamic Computations in Retina , 2018, Trends in Neurosciences.

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

[11]  Yang Li,et al.  Spatiotemporal functional organization of excitatory synaptic inputs onto macaque V1 neurons , 2019, Nature Communications.

[12]  Kenneth D Miller,et al.  Canonical computations of cerebral cortex , 2016, Current Opinion in Neurobiology.

[13]  David Fitzpatrick,et al.  GABAergic Neurons in Ferret Visual Cortex Participate in Functionally Specific Networks , 2017, Neuron.

[14]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

[15]  K. Svoboda,et al.  Genetic Dissection of Neural Circuits , 2008, Neuron.

[16]  M. Wehr,et al.  Rapid Rebalancing of Excitation and Inhibition by Cortical Circuitry , 2018, Neuron.

[17]  H. Adesnik.  Synaptic Mechanisms of Feature Coding in the Visual Cortex of Awake Mice , 2017, Neuron.

[18]  Sonja B. Hofer,et al.  Synaptic organization of visual space in primary visual cortex , 2017, Nature.

[19]  Kevin L. Briggman,et al.  Neural mechanisms of contextual modulation in the retinal direction selective circuit , 2019, Nature Communications.

[20]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

[21]  M. Carandini,et al.  Inhibition dominates sensory responses in awake cortex , 2012, Nature.

[22]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[23]  Jessica A. Cardin,et al.  Functional flexibility in cortical circuits , 2019, Current Opinion in Neurobiology.

[24]  K. Miller,et al.  Neural noise can explain expansive, power-law nonlinearities in neural response functions. , 2002, Journal of neurophysiology.

[25]  Laura Waller,et al.  Precise multimodal optical control of neural ensemble activity , 2018, Nature Neuroscience.

[26]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[27]  Jeffry S. Isaacson,et al.  Network-Level Control of Frequency Tuning in Auditory Cortex , 2017, Neuron.

[28]  Eero P. Simoncelli,et al.  Origin and Function of Tuning Diversity in Macaque Visual Cortex , 2015, Neuron.

[29]  Paul Miller,et al.  Cortical amplification models of experience-dependent development of selective columns and response sparsification. , 2017, Journal of neurophysiology.

[30]  Grace W. Lindsay,et al.  Parallel processing by cortical inhibition enables context-dependent behavior , 2016, Nature Neuroscience.

[31]  M. Histed.  Feedforward Inhibition Allows Input Summation to Vary in Recurrent Cortical Networks , 2017, eNeuro.

[32]  Brett J. Graham,et al.  Anatomy and function of an excitatory network in the visual cortex , 2016, Nature.

[33]  Judit K. Makara,et al.  Global and Multiplexed Dendritic Computations under In Vivo-like Conditions , 2018, Neuron.

[34]  K. Martin,et al.  Local Circuits for Contrast Normalization and Adaptation Investigated with Two-Photon Imaging in Cat Primary Visual Cortex , 2015, The Journal of Neuroscience.

[35]  Pierre Yger,et al.  Multiplexed computations in retinal ganglion cells of a single type , 2016, Nature Communications.

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

[37]  Jeremy Freeman,et al.  Technologies for imaging neural activity in large volumes , 2016, Nature Neuroscience.

[38]  D. Fitzpatrick,et al.  Cortical neuron response selectivity derives from strength in numbers of synapses , 2019, bioRxiv.

[39]  Nicholas J. Priebe,et al.  Mechanisms of Neuronal Computation in Mammalian Visual Cortex , 2012, Neuron.

[40]  Selmaan N. Chettih,et al.  Single-neuron perturbations reveal feature-specific competition in V1 , 2019, Nature.

[41]  D. Fitzpatrick,et al.  Functional Logic of Layer 2/3 Inhibitory Connectivity in the Ferret Visual Cortex , 2019, Neuron.

[42]  C. Koch,et al.  The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[44]  D. R. Muir,et al.  Functional organization of excitatory synaptic strength in primary visual cortex , 2015, Nature.

[45]  Balázs Rózsa,et al.  Single-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules , 2015, Science.

[46]  David Fitzpatrick,et al.  Local Order within Global Disorder: Synaptic Architecture of Visual Space , 2017, Neuron.