A transformation from temporal to ensemble coding in a model of piriform cortex

Different coding strategies are used to represent odor information at various stages of the mammalian olfactory system. A temporal latency code represents odor identity in olfactory bulb (OB), but this temporal information is discarded in piriform cortex (PCx) where odor identity is instead encoded through ensemble membership. We developed a spiking PCx network model to understand how this transformation is implemented. In the model, the impact of OB inputs activated earliest after inhalation is amplified within PCx by diffuse recurrent collateral excitation, which then recruits strong, sustained feedback inhibition that suppresses the impact of later-responding glomeruli. We model increasing odor concentrations by decreasing glomerulus onset latencies while preserving their activation sequences. This produces a multiplexed cortical odor code in which activated ensembles are robust to concentration changes while concentration information is encoded through population synchrony. Our model demonstrates how PCx circuitry can implement multiplexed ensemble-identity/temporal-concentration odor coding.

[1]  Alexei A. Koulakov,et al.  A primacy code for odor identity , 2017, Nature Communications.

[2]  Thomas Deneux,et al.  Odor identity coding by distributed ensembles of neurons in the mouse olfactory cortex , 2017, eLife.

[3]  Kevin M Franks,et al.  Complementary codes for odor identity and intensity in olfactory cortex , 2017, eLife.

[4]  Sandeep Robert Datta,et al.  Population Coding in an Innately Relevant Olfactory Area , 2017, Neuron.

[5]  Maoz Shamir,et al.  A Readout Mechanism for Latency Codes , 2016, Front. Comput. Neurosci..

[6]  Kyle R. Hansen,et al.  Control of Mitral/Tufted Cell Output by Selective Inhibition among Olfactory Bulb Glomeruli , 2016, Neuron.

[7]  Ian R. Wickersham,et al.  Massive normalization of olfactory bulb output in mice with a 'monoclonal nose' , 2016, eLife.

[8]  Anne-Marie M. Oswald,et al.  Balanced feedforward inhibition and dominant recurrent inhibition in olfactory cortex , 2016, Proceedings of the National Academy of Sciences.

[9]  Tatsuo K Sato,et al.  An excitatory basis for divisive normalization in visual cortex , 2016, Nature Neuroscience.

[10]  Yevgeniy B. Sirotin,et al.  Neural Coding of Perceived Odor Intensity1,2,3 , 2015, eNeuro.

[11]  Dmitry Rinberg,et al.  Novel Behavioral Paradigm Reveals Lower Temporal Limits on Mouse Olfactory Decisions , 2015, The Journal of Neuroscience.

[12]  H. Matsunami,et al.  Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo , 2015, Nature Neuroscience.

[13]  Hassana K. Oyibo,et al.  An Interglomerular Circuit Gates Glomerular Output and Implements Gain Control in the Mouse Olfactory Bulb , 2015, Neuron.

[14]  Gonzalo H. Otazu,et al.  Cortical Feedback Decorrelates Olfactory Bulb Output in Awake Mice , 2015, Neuron.

[15]  J. Isaacson,et al.  Somatostatin-expressing interneurons provide subtractive inhibition and regulate sensory response fidelity in olfactory cortex , 2015, Nature Neuroscience.

[16]  P. Glimcher,et al.  Dynamic Divisive Normalization Predicts Time-Varying Value Coding in Decision-Related Circuits , 2014, The Journal of Neuroscience.

[17]  John Lisman,et al.  A network that performs brute-force conversion of a temporal sequence to a spatial pattern: relevance to odor recognition , 2014, Front. Comput. Neurosci..

[18]  “Silent” mitral cells dominate odor responses in the olfactory bulb of awake mice , 2014, Nature Neuroscience.

[19]  N. Uchida,et al.  Coding and transformations in the olfactory system. , 2014, Annual review of neuroscience.

[20]  Stefano Panzeri,et al.  Reading spike timing without a clock: intrinsic decoding of spike trains , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  John M. Bekkers,et al.  Neurons and circuits for odor processing in the piriform cortex , 2013, Trends in Neurosciences.

[22]  Hongkui Zeng,et al.  Olfactory cortical neurons read out a relative time code in the olfactory bulb , 2013, Nature Neuroscience.

[23]  H. Sompolinsky,et al.  Computing Complex Visual Features with Retinal Spike Times , 2013, PloS one.

[24]  Jeffry S. Isaacson,et al.  Cortical Feedback Control of Olfactory Bulb Circuits , 2012, Neuron.

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

[26]  Andreas T. Schaefer,et al.  Two Distinct Channels of Olfactory Bulb Output , 2012, Neuron.

[27]  Naoshige Uchida,et al.  Odor Representations in Olfactory Cortex: Distributed Rate Coding and Decorrelated Population Activity , 2012, Neuron.

[28]  Troy W. Margrie,et al.  Psychophysical properties of odor processing can be quantitatively described by relative action potential latency patterns in mitral and tufted cells , 2012, Front. Syst. Neurosci..

[29]  Norimitsu Suzuki,et al.  Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex , 2012, The Journal of Neuroscience.

[30]  Alan Carleton,et al.  Encoding Odorant Identity by Spiking Packets of Rate-Invariant Neurons in Awake Mice , 2012, PloS one.

[31]  T. A. Cleland,et al.  Sequential mechanisms underlying concentration invariance in biological olfaction , 2011, Front. Neuroeng..

[32]  M. Carandini,et al.  Normalization as a canonical neural computation , 2011, Nature Reviews Neuroscience.

[33]  Matthew C Smear,et al.  Perception of sniff phase in mouse olfaction , 2011, Nature.

[34]  Donald A. Wilson,et al.  Cortical Processing of Odor Objects , 2011, Neuron.

[35]  Jeffry S. Isaacson,et al.  A Major Role for Intracortical Circuits in the Strength and Tuning of Odor-Evoked Excitation in Olfactory Cortex , 2011, Neuron.

[36]  S. Siegelbaum,et al.  Recurrent Circuitry Dynamically Shapes the Activation of Piriform Cortex , 2011, Neuron.

[37]  Matthew C Smear,et al.  Precise olfactory responses tile the sniff cycle , 2011, Nature Neuroscience.

[38]  Alan R Palmer,et al.  First Spike Latency Code for Interaural Phase Difference Discrimination in the Guinea Pig Inferior Colliculus , 2011, The Journal of Neuroscience.

[39]  T. Cutforth,et al.  Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons , 2011, Nature.

[40]  S. R. Datta,et al.  Distinct representations of olfactory information in different cortical centres , 2011, Nature.

[41]  Michael D. Ehlers,et al.  Neural Circuit Mechanisms for Pattern Detection and Feature Combination in Olfactory Cortex , 2011, Neuron.

[42]  Ian R. Wickersham,et al.  Cortical representations of olfactory input by trans-synaptic tracing , 2011, Nature.

[43]  William Wisden,et al.  Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory , 2011, Nature Neuroscience.

[44]  Minmin Luo,et al.  Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice , 2010, The Journal of Neuroscience.

[45]  Naoshige Uchida,et al.  Robust Odor Coding via Inhalation-Coupled Transient Activity in the Mammalian Olfactory Bulb , 2010, Neuron.

[46]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[47]  Massimo Scanziani,et al.  Pyramidal Cells in Piriform Cortex Receive Convergent Input from Distinct Olfactory Bulb Glomeruli , 2010, The Journal of Neuroscience.

[48]  F. Wolf,et al.  Olfactory Coding with Patterns of Response Latencies , 2010, Neuron.

[49]  Jeffry S. Isaacson,et al.  From Dendrite to Soma: Dynamic Routing of Inhibition by Complementary Interneuron Microcircuits in Olfactory Cortex , 2010, Neuron.

[50]  Norimitsu Suzuki,et al.  Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex. , 2010, Cerebral cortex.

[51]  C. Poo,et al.  Odor representations in olfactory cortex , 2010 .

[52]  Alan Carleton,et al.  Temporal Coding in Olfaction , 2010 .

[53]  A. Menini The Neurobiology of Olfaction , 2009 .

[54]  Dan D. Stettler,et al.  Representations of Odor in the Piriform Cortex , 2009, Neuron.

[55]  J. Isaacson,et al.  Odor Representations in Olfactory Cortex: “Sparse” Coding, Global Inhibition, and Oscillations , 2009, Neuron.

[56]  N. Kopell,et al.  Olfactory Oscillations: the What, How and What For , 2022 .

[57]  N. Schoppa,et al.  GABAergic Circuits Control Input–Spike Coupling in the Piriform Cortex , 2008, The Journal of Neuroscience.

[58]  Ryan M Carey,et al.  Rapid Encoding and Perception of Novel Odors in the Rat , 2008, PLoS biology.

[59]  Alan Carleton,et al.  Dynamic Ensemble Odor Coding in the Mammalian Olfactory Bulb: Sensory Information at Different Timescales , 2008, Neuron.

[60]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[61]  Troy W. Margrie,et al.  Spatiotemporal representations in the olfactory system , 2007, Trends in Neurosciences.

[62]  Donald A Wilson,et al.  Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex , 2007, The Journal of Neuroscience.

[63]  Norimitsu Suzuki,et al.  Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex , 2006, The Journal of Neuroscience.

[64]  A. Gelperin,et al.  Speed-Accuracy Tradeoff in Olfaction , 2006, Neuron.

[65]  Troy W. Margrie,et al.  Neuronal Oscillations Enhance Stimulus Discrimination by Ensuring Action Potential Precision , 2006, PLoS Biology.

[66]  Kevin M. Franks,et al.  Strong Single-Fiber Sensory Inputs to Olfactory Cortex: Implications for Olfactory Coding , 2006, Neuron.

[67]  N. Schoppa,et al.  Synchronization of Olfactory Bulb Mitral Cells by Precisely Timed Inhibitory Inputs , 2006, Neuron.

[68]  Hannah Monyer,et al.  Connexin36 Mediates Spike Synchrony in Olfactory Bulb Glomeruli , 2005, Neuron.

[69]  Andreas T. Schaefer,et al.  Maintaining Accuracy at the Expense of Speed Stimulus Similarity Defines Odor Discrimination Time in Mice , 2004, Neuron.

[70]  Z. Mainen,et al.  Speed and accuracy of olfactory discrimination in the rat , 2003, Nature Neuroscience.

[71]  Jianhua Cang,et al.  In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb , 2003, The Journal of Neuroscience.

[72]  L. Haberly,et al.  Odor‐evoked activity is spatially distributed in piriform cortex , 2003, The Journal of comparative neurology.

[73]  Andreas T. Schaefer,et al.  Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system , 2003, The Journal of physiology.

[74]  A. Grinvald,et al.  Spatio-Temporal Dynamics of Odor Representations in the Mammalian Olfactory Bulb , 2002, Neuron.

[75]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[76]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.

[77]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[78]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[79]  J. Bower,et al.  Dynamics of Cerebral Cortical Networks , 1998 .

[80]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[81]  Richard Granger,et al.  Effects of LTP on Response Selectivity of Simulated Cortical Neurons , 1996, Journal of Cognitive Neuroscience.

[82]  Michael E. Hasselmo,et al.  Review of Bower and Beeman: The Book of GENESIS: Exploring Realistic Neural Models with the GEneral NEural SImulation System , 1995 .

[83]  M. Hasselmo,et al.  Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  J. J. Hopfield,et al.  Pattern recognition computation using action potential timing for stimulus representation , 1995, Nature.

[85]  M. Hasselmo,et al.  Modulation of associative memory function in a biophysical simulation of rat piriform cortex. , 1994, Journal of neurophysiology.

[86]  L. Haberly,et al.  Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. I. Current source-density analysis. , 1993, Journal of neurophysiology.

[87]  J. Bower,et al.  Cortical oscillations and temporal interactions in a computer simulation of piriform cortex. , 1992, Journal of neurophysiology.

[88]  L. Buck,et al.  A novel multigene family may encode odorant receptors. , 1992, Society of General Physiologists series.

[89]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.