Stimulus dependent diversity and stereotypy in the output of an olfactory functional unit

Olfactory inputs are organized in an array of parallel functional units (glomeruli), each relaying information from sensory neurons that express a given odorant receptor to a small population of output neurons, mitral/tufted (MT) cells. MT cells have complex temporal responses to odorants, but how these diverse responses relate to stimulus features is not known. We recorded in awake mice responses from “sister” MT cells that receive input from a functionally-characterized, genetically identified glomerulus, corresponding to a specific receptor (M72). Despite receiving similar inputs, sister MT cells exhibited temporally diverse, concentration variant, excitatory and inhibitory responses to most M72 ligands. In contrast, the strongest known ligand for M72 elicited temporally-stereotyped, early excitatory responses in all sister MT cells that persisted across all odor concentrations. Our data demonstrate that information about ligand affinity is encoded in the collective stereotypy or diversity of activity among sister MT cells within a glomerular functional unit in concentration-independent manner.

[1]  R. Tsien,et al.  Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein , 2004, Nature Biotechnology.

[2]  Troy W. Margrie,et al.  A biophysical signature of network affiliation and sensory processing in mitral cells , 2012, Nature.

[3]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[4]  Maneesh Sahani,et al.  Evidence Optimization Techniques for Estimating Stimulus-Response Functions , 2002, NIPS.

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

[6]  C. Schreiner,et al.  Organization of inhibitory frequency receptive fields in cat primary auditory cortex. , 1999, Journal of neurophysiology.

[7]  Mijung Park,et al.  Bayesian inference for low rank spatiotemporal neural receptive fields , 2013, NIPS.

[8]  H. K. Hartline,et al.  INHIBITORY INTERACTION OF RECEPTOR UNITS IN THE EYE OF LIMULUS , 1957, The Journal of general physiology.

[9]  Veronica Egger,et al.  Dynamic connectivity in the mitral cell-granule cell microcircuit. , 2006, Seminars in cell & developmental biology.

[10]  James M. Jeanne,et al.  Convergence, Divergence, and Reconvergence in a Feedforward Network Improves Neural Speed and Accuracy , 2015, Neuron.

[11]  Philippe Litaudon,et al.  Respiratory modulation of olfactory neurons in the rodent brain. , 2006, Chemical senses.

[12]  Praveen Sethupathy,et al.  Non-topographical contrast enhancement in the olfactory bulb , 2006, BMC Neuroscience.

[13]  Shawn R. Olsen,et al.  Divisive Normalization in Olfactory Population Codes , 2010, Neuron.

[14]  J. Reisert,et al.  Olfactory receptor neuron responses coding for rapid odour sampling , 2011, The Journal of physiology.

[15]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[16]  Peter Mombaerts,et al.  Odorant Receptor Expression Defines Functional Units in the Mouse Olfactory System , 2002, The Journal of Neuroscience.

[17]  Kai Zhao,et al.  Airflow and nanoparticle deposition in rat nose under various breathing and sniffing conditions: a computational evaluation of the unsteady effect. , 2010, Journal of aerosol science.

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

[19]  Nathaniel N. Urban,et al.  Lateral inhibition in the olfactory bulb and in olfaction , 2002, Physiology & Behavior.

[20]  A. Holley,et al.  Convergence in the olfactory system: quantitative aspects of odour sensitivity. , 1978, Journal of theoretical biology.

[21]  T. Komiyama,et al.  Parvalbumin-Expressing Interneurons Linearly Control Olfactory Bulb Output , 2013, Neuron.

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

[23]  Steve M. Potter,et al.  Structure and Emergence of Specific Olfactory Glomeruli in the Mouse , 2001, The Journal of Neuroscience.

[24]  Jie Tan,et al.  Odor Information Processing by the Olfactory Bulb Analyzed in Gene-Targeted Mice , 2010, Neuron.

[25]  Gordon M Shepherd,et al.  The olfactory glomerulus: A cortical module with specific functions , 2005, Journal of neurocytology.

[26]  Matt Wachowiak,et al.  In Vivo Imaging of Neuronal Activity by Targeted Expression of a Genetically Encoded Probe in the Mouse , 2004, Neuron.

[27]  L. Paninski Maximum likelihood estimation of cascade point-process neural encoding models , 2004, Network.

[28]  Tatsuya Yamasoba,et al.  Odorant Response Properties of Individual Neurons in an Olfactory Glomerular Module , 2013, Neuron.

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

[30]  O. Creutzfeldt,et al.  Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. , 1977, Journal of neurophysiology.

[31]  W. Spencer,et al.  Cutaneous masking. II. Geometry of excitatory andinhibitory receptive fields of single units in somatosensory cortex of the cat. , 1979, Journal of neurophysiology.

[32]  Ryan M Carey,et al.  Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. , 2009, Journal of neurophysiology.

[33]  Jennifer D Whitesell,et al.  Interglomerular Lateral Inhibition Targeted on External Tufted Cells in the Olfactory Bulb , 2013, The Journal of Neuroscience.

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

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

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

[37]  Dmitry Rinberg,et al.  Multiple perceptible signals from a single olfactory glomerulus , 2014, Nature Neuroscience.

[38]  Susana Q. Lima,et al.  PINP: A New Method of Tagging Neuronal Populations for Identification during In Vivo Electrophysiological Recording , 2009, PloS one.

[39]  M. M. Mozell,et al.  Evidence for a Chromatographic Model of Olfaction , 1970, The Journal of general physiology.

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

[41]  E I Knudsen,et al.  Center-surround organization of auditory receptive fields in the owl. , 1978, Science.

[42]  Adam Dewan,et al.  Uncoupling stimulus specificity and glomerular position in the mouse olfactory system , 2012, Molecular and Cellular Neuroscience.

[43]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[44]  Yevgeniy B. Sirotin,et al.  Single Scale for Odor Intensity in Rat Olfaction , 2014, Current Biology.

[45]  Minmin Luo,et al.  Response Correlation Maps of Neurons in the Mammalian Olfactory Bulb , 2001, Neuron.

[46]  J. Greer,et al.  Targeting genes for self-excision in the germ line. , 1999, Genes & development.

[47]  M. Sur Receptive fields of neurons in areas 3b and 1 of somatosensory cortex in monkeys , 1980, Brain Research.

[48]  Lynn Hazan,et al.  Klusters, NeuroScope, NDManager: A free software suite for neurophysiological data processing and visualization , 2006, Journal of Neuroscience Methods.

[49]  N. Urban,et al.  Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content , 2010, Nature Neuroscience.

[50]  Detlev Schild,et al.  Odor coding by modules of coherent mitral/tufted cells in the vertebrate olfactory bulb , 2009, Proceedings of the National Academy of Sciences.

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

[52]  Mijung Park,et al.  Receptive Field Inference with Localized Priors , 2011, PLoS Comput. Biol..

[53]  Antoniu L. Fantana,et al.  Rat Olfactory Bulb Mitral Cells Receive Sparse Glomerular Inputs , 2008, Neuron.

[54]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

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

[56]  Upinder S Bhalla,et al.  Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse , 2010, Nature Neuroscience.

[57]  L. Cohen,et al.  Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. , 2006, Journal of neurophysiology.

[58]  Gordon M Shepherd,et al.  Viral tracing identifies distributed columnar organization in the olfactory bulb , 2006, Proceedings of the National Academy of Sciences.

[59]  Bert Sakmann,et al.  Reciprocal intraglomerular excitation and intra‐ and interglomerular lateral inhibition between mouse olfactory bulb mitral cells , 2002, The Journal of physiology.

[60]  Joshua T. Dudman,et al.  RIVETS: A Mechanical System for In Vivo and In Vitro Electrophysiology and Imaging , 2014, PloS one.