Coding of odors by temporal binding within a model network of the locust antennal lobe

The locust olfactory system interfaces with the external world through antennal receptor neurons (ORNs), which represent odors in a distributed, combinatorial manner. ORN axons bundle together to form the antennal nerve, which relays sensory information centrally to the antennal lobe (AL). Within the AL, an odor generates a dynamically evolving ensemble of active cells, leading to a stimulus-specific temporal progression of neuronal spiking. This experimental observation has led to the hypothesis that an odor is encoded within the AL by a dynamically evolving trajectory of projection neuron (PN) activity that can be decoded piecewise to ascertain odor identity. In order to study information coding within the locust AL, we developed a scaled-down model of the locust AL using Hodgkin–Huxley-type neurons and biologically realistic connectivity parameters and current components. Using our model, we examined correlations in the precise timing of spikes across multiple neurons, and our results suggest an alternative to the dynamic trajectory hypothesis. We propose that the dynamical interplay of fast and slow inhibition within the locust AL induces temporally stable correlations in the spiking activity of an odor-dependent neural subset, giving rise to a temporal binding code that allows rapid stimulus detection by downstream elements.

[1]  Aaditya V. Rangan,et al.  A large-scale model of the locust antennal lobe , 2009, Journal of Computational Neuroscience.

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

[3]  B. Hansson,et al.  Function and morphology of the antennal lobe: new developments. , 2000, Annual review of entomology.

[4]  G Laurent,et al.  Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. , 1993, Journal of neurophysiology.

[5]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[6]  H. Le Corronc,et al.  Differential sensitivity of two insect GABA-gated chloride channels to dieldrin, fipronil and picrotoxinin. , 2002, Journal of insect physiology.

[7]  Hong Lei,et al.  Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons , 2002, Nature Neuroscience.

[8]  G. Laurent,et al.  Transient Dynamics versus Fixed Points in Odor Representations by Locust Antennal Lobe Projection Neurons , 2005, Neuron.

[9]  T J Sejnowski,et al.  Cellular and network models for intrathalamic augmenting responses during 10-Hz stimulation. , 1998, Journal of neurophysiology.

[10]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[11]  T. Powell,et al.  Ultrastructural features of the sensori-motor cortex of the primate. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  G. Laurent,et al.  Short-term memory in olfactory network dynamics , 1999, Nature.

[13]  W Singer,et al.  Role of the temporal domain for response selection and perceptual binding. , 1997, Cerebral cortex.

[14]  J. Hildebrand,et al.  Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles , 2000, Nature Neuroscience.

[15]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[16]  M. Stopfer,et al.  Functional Analysis of a Higher Olfactory Center, the Lateral Horn , 2012, The Journal of Neuroscience.

[17]  N. Vickers,et al.  Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli , 1998, The Journal of comparative neurology.

[18]  Gilles Laurent,et al.  A Simple Connectivity Scheme for Sparse Coding in an Olfactory System , 2007, The Journal of Neuroscience.

[19]  G. Laurent,et al.  Temporal Representations of Odors in an Olfactory Network , 1996, The Journal of Neuroscience.

[20]  G. Laurent,et al.  Encoding of Olfactory Information with Oscillating Neural Assemblies , 1994, Science.

[21]  L. Cohen,et al.  Representation of Odorants by Receptor Neuron Input to the Mouse Olfactory Bulb , 2001, Neuron.

[22]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[23]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[24]  A Combinatorial Model of Odor Discrimination Using a Small Array of Contiguous, Chemically Defined Glomeruli , 1998, Annals of the New York Academy of Sciences.

[25]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[26]  Dominique Martinez,et al.  A Model of Stimulus-Specific Neural Assemblies in the Insect Antennal Lobe , 2008, PLoS Comput. Biol..

[27]  V. Jayaraman,et al.  Encoding and Decoding of Overlapping Odor Sequences , 2006, Neuron.

[28]  Y. Hamasaka,et al.  γ‐Aminobutyric acid (GABA) signaling components in Drosophila: Immunocytochemical localization of GABAB receptors in relation to the GABAA receptor subunit RDL and a vesicular GABA transporter , 2007, The Journal of comparative neurology.

[29]  T. Sejnowski,et al.  Model of Transient Oscillatory Synchronization in the Locust Antennal Lobe , 2001, Neuron.

[30]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[31]  G. Laurent,et al.  Normalization for Sparse Encoding of Odors by a Wide-Field Interneuron , 2011, Science.

[32]  G Laurent,et al.  Spatiotemporal structure of olfactory inputs to the mushroom bodies. , 1998, Learning & memory.

[33]  P Duchamp-Viret,et al.  Peripheral Odor Coding in the Rat and Frog: Quality and Intensity Specification , 2000, The Journal of Neuroscience.

[34]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[35]  J. Hildebrand,et al.  Postembryonic development of the olfactory system in the moth Manduca sexta: primary-afferent control of glomerular development. , 1997, Seminars in cell & developmental biology.

[36]  G. Laurent,et al.  Who reads temporal information contained across synchronized and oscillatory spike trains? , 1998, Nature.

[37]  B. Ache,et al.  Olfaction: Diverse Species, Conserved Principles , 2005, Neuron.

[38]  J. Hildebrand,et al.  Structure and function of the deutocerebrum in insects. , 1989, Annual review of entomology.

[39]  W. Singer,et al.  Precisely Synchronized Oscillatory Firing Patterns Require Electroencephalographic Activation , 1999, The Journal of Neuroscience.

[40]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[41]  J. Hildebrand,et al.  Enantioselectivity of Projection Neurons Innervating Identified Olfactory Glomeruli , 2004, The Journal of Neuroscience.

[42]  G. Laurent,et al.  Relationship between Afferent and Central Temporal Patterns in the Locust Olfactory System , 1999, The Journal of Neuroscience.

[43]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[44]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[45]  T. Sejnowski,et al.  Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. , 1996, Journal of neurophysiology.

[46]  J R Huguenard,et al.  A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. , 1991, Journal of neurophysiology.

[47]  J. Rybak,et al.  Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera , 2005, Journal of Comparative Physiology A.

[48]  W. Singer,et al.  Detecting connectedness. , 1998, Cerebral cortex.

[49]  Terrence J. Sejnowski,et al.  Model of Cellular and Network Mechanisms for Odor-Evoked Temporal Patterning in the Locust Antennal Lobe , 2001, Neuron.

[50]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

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

[52]  C. Koch,et al.  An oscillation-based model for the neuronal basis of attention , 1993, Vision Research.

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

[54]  M. Stopfer,et al.  Encoding a temporally structured stimulus with a temporally structured neural representation , 2005, Nature Neuroscience.

[55]  G. Laurent,et al.  GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system , 1996, The Journal of comparative neurology.

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

[57]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[58]  Mark T. Waters,et al.  This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.Thislicensedoesnot permit commercial exploitation or the creation of derivative works without sp , 2009 .

[59]  F. C. Kenyon.  The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda , 1896 .

[60]  T. Bonhoeffer,et al.  Tuning and Topography in an Odor Map on the Rat Olfactory Bulb , 2001, The Journal of Neuroscience.

[61]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[62]  G. Laurent,et al.  Odorant-induced oscillations in the mushroom bodies of the locust , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  G. Laurent,et al.  Distinct Mechanisms for Synchronization and Temporal Patterning of Odor-Encoding Neural Assemblies , 1996, Science.

[64]  S. Buckingham,et al.  Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine. , 1999, Journal of neurophysiology.

[65]  R. Menzel,et al.  Representations of odours and odour mixtures visualized in the honeybee brain , 1997, Nature.