Neurogenesis Drives Stimulus Decorrelation in a Model of the Olfactory Bulb

The reshaping and decorrelation of similar activity patterns by neuronal networks can enhance their discriminability, storage, and retrieval. How can such networks learn to decorrelate new complex patterns, as they arise in the olfactory system? Using a computational network model for the dominant neural populations of the olfactory bulb we show that fundamental aspects of the adult neurogenesis observed in the olfactory bulb – the persistent addition of new inhibitory granule cells to the network, their activity-dependent survival, and the reciprocal character of their synapses with the principal mitral cells – are sufficient to restructure the network and to alter its encoding of odor stimuli adaptively so as to reduce the correlations between the bulbar representations of similar stimuli. The decorrelation is quite robust with respect to various types of perturbations of the reciprocity. The model parsimoniously captures the experimentally observed role of neurogenesis in perceptual learning and the enhanced response of young granule cells to novel stimuli. Moreover, it makes specific predictions for the type of odor enrichment that should be effective in enhancing the ability of animals to discriminate similar odor mixtures.

[1]  Samuel Weiss,et al.  Paternal recognition of adult offspring mediated by newly generated CNS neurons , 2010, Nature Neuroscience.

[2]  M. Grubb,et al.  Turning Astrocytes from the Rostral Migratory Stream into Neurons: A Role for the Olfactory Sensory Organ , 2008, The Journal of Neuroscience.

[3]  F. Jourdan,et al.  Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation , 2006, Neuroscience.

[4]  G. Laurent,et al.  Multiplexing using synchrony in the zebrafish olfactory bulb , 2004, Nature Neuroscience.

[5]  Hideyuki Okano,et al.  Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb , 2006, Genes to cells : devoted to molecular & cellular mechanisms.

[6]  Hiroyuki Manabe,et al.  Elimination of Adult-Born Neurons in the Olfactory Bulb Is Promoted during the Postprandial Period , 2011, Neuron.

[7]  Wolfgang Kelsch,et al.  Sequential development of synapses in dendritic domains during adult neurogenesis , 2008, Proceedings of the National Academy of Sciences.

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

[9]  Donald A. Wilson,et al.  Pattern Separation: A Common Function for New Neurons in Hippocampus and Olfactory Bulb , 2011, Neuron.

[10]  Donald A. Wilson,et al.  Learning to Smell: Olfactory Perception from Neurobiology to Behavior , 2006 .

[11]  Hong-Wei Dong,et al.  Noradrenergic regulation of GABAergic inhibition of main olfactory bulb mitral cells varies as a function of concentration and receptor subtype. , 2009, Journal of neurophysiology.

[12]  C. Greer,et al.  Synaptic Integration of Adult-Generated Olfactory Bulb Granule Cells: Basal Axodendritic Centrifugal Input Precedes Apical Dendrodendritic Local Circuits , 2007, The Journal of Neuroscience.

[13]  Matti Poutanen,et al.  Male pheromone–stimulated neurogenesis in the adult female brain: possible role in mating behavior. , 2007, Nature Neuroscience.

[14]  Christelle Rochefort,et al.  Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory , 2002, The Journal of Neuroscience.

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

[16]  C Giovanni Galizia,et al.  Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. , 2005, Journal of neurophysiology.

[17]  P. Lledo,et al.  Turnover of Newborn Olfactory Bulb Neurons Optimizes Olfaction , 2009, The Journal of Neuroscience.

[18]  Thomas A Cleland,et al.  Olfactory bulb habituation to odor stimuli. , 2010, Behavioral neuroscience.

[19]  Nathalie Mandairon,et al.  Olfactory enrichment improves the recognition of individual components in mixtures , 2006, Physiology & Behavior.

[20]  D. Storm,et al.  Odorant-Induced Activation of Extracellular Signal-Regulated Kinase/Mitogen-Activated Protein Kinase in the Olfactory Bulb Promotes Survival of Newly Formed Granule Cells , 2005, The Journal of Neuroscience.

[21]  Anne Didier,et al.  Acquisition of an Olfactory Associative Task Triggers a Regionalized Down-Regulation of Adult Born Neuron Cell Death , 2011, Front. Neurosci..

[22]  Hermann Riecke,et al.  Mechanisms of pattern decorrelation by recurrent neuronal circuits , 2010, Nature Neuroscience.

[23]  Y. Sato,et al.  An in vitro study of long-term potentiation in the carp (Cyprinus carpio L.) olfactory bulb , 2006, Journal of Comparative Physiology A.

[24]  Leslie M Kay,et al.  A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. , 2010, Journal of neurophysiology.

[25]  L. Abbott,et al.  Generating sparse and selective third-order responses in the olfactory system of the fly , 2010, Proceedings of the National Academy of Sciences.

[26]  Vikrant Kapoor,et al.  Activity-dependent gating of lateral inhibition in the mouse olfactory bulb , 2008, Nature Neuroscience.

[27]  Thomas A Cleland,et al.  Distinct neural mechanisms mediate olfactory memory formation at different timescales. , 2008, Learning & memory.

[28]  Armen Saghatelyan,et al.  Interneurons Produced in Adulthood Are Required for the Normal Functioning of the Olfactory Bulb Network and for the Execution of Selected Olfactory Behaviors , 2009, The Journal of Neuroscience.

[29]  B. Strowbridge,et al.  Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb , 2009, Nature Neuroscience.

[30]  Masahiro Yamaguchi,et al.  Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Bob S Carter,et al.  Adult-Born and Preexisting Olfactory Granule Neurons Undergo Distinct Experience-Dependent Modifications of their Olfactory Responses In Vivo , 2005, The Journal of Neuroscience.

[32]  Arturo Alvarez-Buylla,et al.  Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction , 2002, The Journal of Neuroscience.

[33]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

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

[35]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[36]  P. Brennan,et al.  Mammalian social odours: attraction and individual recognition , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Matthew S. Grubb,et al.  Adult neurogenesis and functional plasticity in neuronal circuits , 2006, Nature Reviews Neuroscience.

[38]  Magdalena Götz,et al.  Distinct Modes of Neuron Addition in Adult Mouse Neurogenesis , 2007, The Journal of Neuroscience.

[39]  P. Lledo,et al.  The how and why of adult neurogenesis , 2007, Journal of Molecular Histology.

[40]  Christiane Linster,et al.  Neurobiology of a simple memory. , 2008, Journal of neurophysiology.

[41]  Anne Didier,et al.  Newborn Neurons in the Olfactory Bulb Selected for Long-Term Survival through Olfactory Learning Are Prematurely Suppressed When the Olfactory Memory Is Erased , 2011, The Journal of Neuroscience.

[42]  Anne Didier,et al.  Consolidation of an Olfactory Memory Trace in the Olfactory Bulb Is Required for Learning-Induced Survival of Adult-Born Neurons and Long-Term Memory , 2010, PloS one.

[43]  Wolfgang Kelsch,et al.  Genetically Increased Cell-Intrinsic Excitability Enhances Neuronal Integration into Adult Brain Circuits , 2010, Neuron.

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

[45]  A. Carleton,et al.  Multiple and Opposing Roles of Cholinergic Transmission in the Main Olfactory Bulb , 1999, The Journal of Neuroscience.

[46]  D. Abrous,et al.  Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date , 2003, Molecular Psychiatry.

[47]  Tsuyoshi Inoue,et al.  Muscarinic Receptor Activation Modulates Granule Cell Excitability and Potentiates Inhibition onto Mitral Cells in the Rat Olfactory Bulb , 2007, The Journal of Neuroscience.

[48]  Nathalie Mandairon,et al.  Enrichment to odors improves olfactory discrimination in adult rats. , 2006, Behavioral neuroscience.

[49]  Jürgen Winkler,et al.  Long‐term survival and cell death of newly generated neurons in the adult rat olfactory bulb , 2002, The European journal of neuroscience.

[50]  F. Kermen,et al.  Learning‐dependent neurogenesis in the olfactory bulb determines long‐term olfactory memory , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[51]  Woong Sun,et al.  Impaired Migration in the Rostral Migratory Stream But Spared Olfactory Function after the Elimination of Programmed Cell Death in Bax Knock-Out Mice , 2007, The Journal of Neuroscience.

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

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

[54]  Marco Sassoè-Pognetto,et al.  Early Synapse Formation in Developing Interneurons of the Adult Olfactory Bulb , 2009, The Journal of Neuroscience.

[55]  Ryoichiro Kageyama,et al.  Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain , 2008, Nature Neuroscience.

[56]  Veronica Egger,et al.  Synaptic sodium spikes trigger long‐lasting depolarizations and slow calcium entry in rat olfactory bulb granule cells , 2008, The European journal of neuroscience.

[57]  Christiane Linster,et al.  Noradrenergic modulation of behavioral odor detection and discrimination thresholds in the olfactory bulb , 2010, The European journal of neuroscience.

[58]  C. Greer,et al.  Adult neurogenesis and the olfactory system , 2009, Progress in Neurobiology.

[59]  Michael Leon,et al.  Chemotopic odorant coding in a mammalian olfactory system , 2007, The Journal of comparative neurology.

[60]  P. Lledo,et al.  Is adult neurogenesis essential for olfaction? , 2011, Trends in Neurosciences.

[61]  Thomas A. Cleland,et al.  Lateral dendritic shunt inhibition can regularize mitral cell spike patterning , 2008, Journal of Computational Neuroscience.

[62]  R. Dolmetsch,et al.  Signaling to the Nucleus by an L-type Calcium Channel-Calmodulin Complex Through the MAP Kinase Pathway , 2001, Science.

[63]  F. Jourdan,et al.  Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice , 2003, Neuroscience.

[64]  Rainer W Friedrich,et al.  Topological Reorganization of Odor Representations in the Olfactory Bulb , 2007, PLoS biology.

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

[66]  Anne Didier,et al.  Odor enrichment increases interneurons responsiveness in spatially defined regions of the olfactory bulb correlated with perception , 2008, Neurobiology of Learning and Memory.

[67]  Christopher Gregg,et al.  Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin , 2003, Science.

[68]  G. Shepherd,et al.  Serial reconstructions of granule cell spines in the mammalian olfactory bulb , 1991, Synapse.

[69]  Guillermo A. Cecchi,et al.  Unsupervised Learning and Adaptation in a Model of Adult Neurogenesis , 2001, Journal of Computational Neuroscience.

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

[71]  Jean-Christophe Olivo-Marin,et al.  Cellular and Behavioral Effects of Cranial Irradiation of the Subventricular Zone in Adult Mice , 2009, PloS one.

[72]  Stuart Firestein,et al.  Ablation of Mouse Adult Neurogenesis Alters Olfactory Bulb Structure and Olfactory Fear Conditioning , 2009, Front. Neurosci..

[73]  D. Abrous,et al.  A Critical Time Window for the Recruitment of Bulbar Newborn Neurons by Olfactory Discrimination Learning , 2011, The Journal of Neuroscience.

[74]  Hermann Riecke,et al.  Pattern orthogonalization via channel decorrelation by adaptive networks , 2009, Journal of Computational Neuroscience.

[75]  Brett A. Johnson,et al.  Relational representation in the olfactory system , 2007, Proceedings of the National Academy of Sciences.

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

[77]  Jean-Christophe Olivo-Marin,et al.  Learning and Survival of Newly Generated Neurons: When Time Matters , 2008, The Journal of Neuroscience.

[78]  Nathalie Mandairon,et al.  Broad activation of the olfactory bulb produces long-lasting changes in odor perception , 2006, Proceedings of the National Academy of Sciences.

[79]  Anne Didier,et al.  Olfactory perceptual learning requires adult neurogenesis , 2009, Proceedings of the National Academy of Sciences.