Odor Representations in Olfactory Cortex: Distributed Rate Coding and Decorrelated Population Activity

VIDEO ABSTRACT How information encoded in neuronal spike trains is used to guide sensory decisions is a fundamental question. In olfaction, a single sniff is sufficient for fine odor discrimination but the neural representations on which olfactory decisions are based are unclear. Here, we recorded neural ensemble activity in the anterior piriform cortex (aPC) of rats performing an odor mixture categorization task. We show that odors evoke transient bursts locked to sniff onset and that odor identity can be better decoded using burst spike counts than by spike latencies or temporal patterns. Surprisingly, aPC ensembles also exhibited near-zero noise correlations during odor stimulation. Consequently, fewer than 100 aPC neurons provided sufficient information to account for behavioral speed and accuracy, suggesting that behavioral performance limits arise downstream of aPC. These findings demonstrate profound transformations in the dynamics of odor representations from the olfactory bulb to cortex and reveal likely substrates for odor-guided decisions.

[1]  Shigeo Abe DrEng.  Pattern Classification , 2001, Springer London.

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

[3]  F. Mechler,et al.  Independent and Redundant Information in Nearby Cortical Neurons , 2001, Science.

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

[5]  David G. Stork,et al.  Pattern Classification , 1973 .

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

[7]  Markus Meister,et al.  Precision and diversity in an odor map on the olfactory bulb , 2009, Nature Neuroscience.

[8]  Daeyeol Lee,et al.  Neural Noise and Movement-Related Codes in the Macaque Supplementary Motor Area , 2003, The Journal of Neuroscience.

[9]  Alan Gelperin,et al.  Sparse Odor Coding in Awake Behaving Mice , 2006, The Journal of Neuroscience.

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

[11]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[12]  N. Uchida,et al.  Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. , 1999, Journal of neurophysiology.

[13]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[14]  W. Newsome,et al.  Context-Dependent Changes in Functional Circuitry in Visual Area MT , 2008, Neuron.

[15]  Gilles Laurent,et al.  Odor- and context-dependent modulation of mitral cell activity in behaving rats , 1999, Nature Neuroscience.

[16]  J. Hertz,et al.  Adjacent visual cortical complex cells share about 20% of their stimulus-related information. , 1996, Cerebral cortex.

[17]  G. DeAngelis,et al.  Contribution of Area MT to Stereoscopic Depth Perception Choice-Related Response Modulations Reflect Task Strategy , 2004, Neuron.

[18]  W. Precht.  The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[19]  M. Wachowiak,et al.  Effect of Sniffing on the Temporal Structure of Mitral/Tufted Cell Output from the Olfactory Bulb , 2011, The Journal of Neuroscience.

[20]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque , 2008 .

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

[22]  Adam Kepecs,et al.  The sniff as a unit of olfactory processing. , 2006, Chemical senses.

[23]  Karl Deisseroth,et al.  Neuronal filtering of multiplexed odour representations , 2011, Nature.

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

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

[26]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[27]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

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

[29]  W. Newsome,et al.  Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation , 2009, The Journal of Neuroscience.

[30]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[31]  勇一 作村,et al.  Biophysics of Computation , 2001 .

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

[33]  Richard Granger,et al.  Short-Latency Single Unit Processing in Olfactory Cortex , 1991, Journal of Cognitive Neuroscience.

[34]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[35]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

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

[37]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

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

[39]  Yong Gu,et al.  Perceptual Learning Reduces Interneuronal Correlations in Macaque Visual Cortex , 2011, Neuron.

[40]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[41]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[42]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[43]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[44]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

[45]  T. A. Harrison,et al.  Discrimination among odorants by single neurons of the rat olfactory bulb. , 1989, Journal of neurophysiology.

[46]  H Eichenbaum,et al.  Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. , 1995, Journal of neurophysiology.

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

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

[49]  Z. Mainen,et al.  Early events in olfactory processing. , 2006, Annual review of neuroscience.

[50]  Eric R. Ziegel,et al.  The Elements of Statistical Learning , 2003, Technometrics.

[51]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

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

[53]  H. Ojima,et al.  The trajectory of mitral cell axons in the rabbit olfactory cortex revealed by intracellular HRP injection , 1984, The Journal of comparative neurology.

[54]  W. Welker.  Analysis of Sniffing of the Albino Rat 1) , 1964 .

[55]  TJ Gawne,et al.  How independent are the messages carried by adjacent inferior temporal cortical neurons? , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[57]  J. Kauer,et al.  Patterns of intracellular potentials in salamander mitral/tufted cells in response to odor stimulation. , 1989, Journal of neurophysiology.

[58]  Adam Kepecs,et al.  Rapid and precise control of sniffing during olfactory discrimination in rats. , 2007, Journal of neurophysiology.

[59]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

[60]  M. Meredith,et al.  Patterned response to odor in mammalian olfactory bulb: the influence of intensity. , 1986, Journal of neurophysiology.

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

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

[63]  Wei R. Chen,et al.  Differential Axonal Projection of Mitral and Tufted Cells in the Mouse Main Olfactory System , 2010, Front. Neural Circuits.

[64]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[65]  G. Laurent,et al.  Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input , 2004, The Journal of Neuroscience.

[66]  D. Wilson,et al.  Habituation of odor responses in the rat anterior piriform cortex. , 1998, Journal of neurophysiology.

[67]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[68]  A. P. Georgopoulos,et al.  Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex , 1998, The Journal of Neuroscience.

[69]  F. Macrides,et al.  Olfactory Bulb Units: Activity Correlated with Inhalation Cycles and Odor Quality , 1972, Science.

[70]  M. Wachowiak.  All in a Sniff: Olfaction as a Model for Active Sensing , 2011, Neuron.

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

[72]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[73]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[74]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[77]  Rachel I. Wilson,et al.  Origins of correlated activity in an olfactory circuit , 2009, Nature Neuroscience.

[78]  M. Laubach,et al.  Redundancy and Synergy of Neuronal Ensembles in Motor Cortex , 2005, The Journal of Neuroscience.

[79]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[80]  Shawn R. Olsen,et al.  Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations , 2007, Nature Neuroscience.

[81]  L. Haberly,et al.  Summed potentials evoked in opossum prepyriform cortex. , 1973, Journal of neurophysiology.

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

[83]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[84]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[85]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[86]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

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

[88]  A. Parker,et al.  Perceptually Bistable Three-Dimensional Figures Evoke High Choice Probabilities in Cortical Area MT , 2001, The Journal of Neuroscience.

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

[90]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[91]  M. Quirk,et al.  Representation of Spatial Goals in Rat Orbitofrontal Cortex , 2006, Neuron.

[92]  H. Sompolinsky,et al.  Population coding in neuronal systems with correlated noise. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[93]  Xin Huang,et al.  Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. , 2009, Journal of neurophysiology.

[94]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[95]  Christian W. Eurich,et al.  Representational Accuracy of Stochastic Neural Populations , 2002, Neural Computation.

[96]  Eric Shea-Brown,et al.  Stimulus-Dependent Correlations and Population Codes , 2008, Neural Computation.