Physiology of Layer 5 Pyramidal Neurons in Mouse Primary Visual Cortex: Coincidence Detection through Bursting

L5 pyramidal neurons are the only neocortical cell type with dendrites reaching all six layers of cortex, casting them as one of the main integrators in the cortical column. What is the nature and mode of computation performed in mouse primary visual cortex (V1) given the physiology of L5 pyramidal neurons? First, we experimentally establish active properties of the dendrites of L5 pyramidal neurons of mouse V1 using patch-clamp recordings. Using a detailed multi-compartmental model, we show this physiological setup to be well suited for coincidence detection between basal and apical tuft inputs by controlling the frequency of spike output. We further show how direct inhibition of calcium channels in the dendrites modulates such coincidence detection. To establish the singe-cell computation that this biophysics supports, we show that the combination of frequency-modulation of somatic output by tuft input and (simulated) calcium-channel blockage functionally acts as a composite sigmoidal function. Finally, we explore how this computation provides a mechanism whereby dendritic spiking contributes to orientation tuning in pyramidal neurons.

[1]  Henry Markram,et al.  Models of Neocortical Layer 5b Pyramidal Cells Capturing a Wide Range of Dendritic and Perisomatic Active Properties , 2011, PLoS Comput. Biol..

[2]  M. Larkum,et al.  NMDA spikes enhance action potential generation during sensory input , 2014, Nature Neuroscience.

[3]  J. Price.  :Allen Reference Atlas: A Digital Color Brain Atlas of the C57BL/6J Male Mouse , 2008 .

[4]  L. Maffei,et al.  Two firing patterns in the discharge of complex cells encoding different attributes of the visual stimulus , 2004, Experimental Brain Research.

[5]  C. Koch,et al.  Multiplicative computation in a visual neuron sensitive to looming , 2002, Nature.

[6]  B. Sakmann,et al.  High frequency action potential bursts (≥ 100 Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex , 2008, The Journal of physiology.

[7]  Nathan R. Wilson,et al.  El-Boustani et al. reply , 2014, Nature.

[8]  Srdjan D Antic,et al.  Voltage and calcium transients in basal dendrites of the rat prefrontal cortex , 2007, The Journal of physiology.

[9]  A. Burkhalter,et al.  A Polysynaptic Feedback Circuit in Rat Visual Cortex , 1997, The Journal of Neuroscience.

[10]  D H Hubel,et al.  Visual responses in V1 of freely viewing monkeys. , 1996, Cold Spring Harbor symposia on quantitative biology.

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

[12]  Masanori Murayama,et al.  Inhibitory Regulation of Dendritic Activity in vivo , 2012, Front. Neural Circuits.

[13]  M. Larkum,et al.  Properties of Layer 6 Pyramidal Neuron Apical Dendrites , 2010, The Journal of Neuroscience.

[14]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[15]  Arthur W. Wetzel,et al.  Network anatomy and in vivo physiology of visual cortical neurons , 2011, Nature.

[16]  Adam G. Carter,et al.  GABAB Receptor Modulation of Voltage-Sensitive Calcium Channels in Spines and Dendrites , 2011, The Journal of Neuroscience.

[17]  Spencer L. Smith,et al.  Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo , 2013, Nature.

[18]  N. Spruston,et al.  Action potential initiation and backpropagation in neurons of the mammalian CNS , 1997, Trends in Neurosciences.

[19]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

[20]  Jude F. Mitchell,et al.  Attentional Modulation of Firing Rate Varies with Burstiness across Putative Pyramidal Neurons in Macaque Visual Area V4 , 2011, The Journal of Neuroscience.

[21]  Karl Deisseroth,et al.  Activation of Specific Interneurons Improves V1 Feature Selectivity and Visual Perception , 2012, Nature.

[22]  B. Sakmann,et al.  Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  J. Seamans,et al.  Contributions of Voltage-Gated Ca2+ Channels in the Proximal versus Distal Dendrites to Synaptic Integration in Prefrontal Cortical Neurons , 1997, The Journal of Neuroscience.

[26]  Matthew E. Larkum,et al.  The GABAB1b Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons , 2006, Neuron.

[27]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[28]  Stephen R. Williams,et al.  Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons , 1999, The Journal of physiology.

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

[30]  Hysell V. Oviedo,et al.  Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite , 2002, Nature Neuroscience.

[31]  Andreas Burkhalter,et al.  Microcircuitry of forward and feedback connections within rat visual cortex , 1996, The Journal of comparative neurology.

[32]  Lindsey L. Glickfeld,et al.  Cortico-cortical projections in mouse visual cortex are functionally target specific , 2013, Nature Neuroscience.

[33]  B. Sakmann,et al.  Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[34]  Hong Wei Dong,et al.  Allen reference atlas : a digital color brain atlas of the C57Black/6J male mouse , 2008 .

[35]  B. Sakmann,et al.  Dendritic Spikes in Apical Dendrites of Neocortical Layer 2/3 Pyramidal Neurons , 2007, The Journal of Neuroscience.

[36]  M. Carandini,et al.  Atallah et al. reply , 2014, Nature.

[37]  D. Johnston,et al.  Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. , 1998, Annual review of physiology.

[38]  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.

[39]  M. Carandini.  From circuits to behavior: a bridge too far? , 2012, Nature Neuroscience.

[40]  Yang Dan,et al.  Interneuron subtypes and orientation tuning , 2014, Nature.

[41]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[42]  C. Niell,et al.  What can mice tell us about how vision works? , 2011, Trends in Neurosciences.

[43]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.