Model of Cellular and Network Mechanisms for Odor-Evoked Temporal Patterning in the Locust Antennal Lobe

Locust antennal lobe (AL) projection neurons (PNs) respond to olfactory stimuli with sequences of depolarizing and hyperpolarizing epochs, each lasting hundreds of milliseconds. A computer simulation of an AL network was used to test the hypothesis that slow inhibitory connections between local neurons (LNs) and PNs are responsible for temporal patterning. Activation of slow inhibitory receptors on PNs by the same GABAergic synapses that underlie fast oscillatory synchronization of PNs was sufficient to shape slow response modulations. This slow stimulus- and neuron-specific patterning of AL activity was resistant to blockade of fast inhibition. Fast and slow inhibitory mechanisms at synapses between LNs and PNs can thus form dynamical PN assemblies whose elements synchronize transiently and oscillate collectively, as observed not only in the locust AL, but also in the vertebrate olfactory bulb.

[1]  R. Menzel,et al.  The glomerular code for odor representation is species specific in the honeybee Apis mellifera , 1999, Nature Neuroscience.

[2]  Christiane Linster,et al.  A Neural Model of Olfactory Sensory Memory in the Honeybee's Antennal Lobe , 1996, Neural Computation.

[3]  W. Harris,et al.  Conditioned behavior in Drosophila melanogaster. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[4]  I. Meinertzhagen,et al.  Synaptic connections of cholinergic antennal lobe relay neurons innervating the lateral horn neuropile in the brain of Drosophila melanogaster , 2003, The Journal of comparative neurology.

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

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

[7]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

[8]  I. Meinertzhagen,et al.  Synaptic organization of the mushroom body calyx in Drosophila melanogaster , 2002, The Journal of comparative neurology.

[9]  M. Burrows,et al.  NADPH diaphorase histochemistry in the thoracic ganglia of locusts, crickets, and cockroaches: Species differences and the impact of fixation , 1999, The Journal of comparative neurology.

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

[11]  A. Watson,et al.  Synaptic structure, distribution, and circuitry in the central nervous system of the locust and related insects , 2002, Microscopy research and technique.

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

[13]  M. O'Shea,et al.  Nitric oxide compartments in the mushroom bodies of the locust brain , 1998, Neuroreport.

[14]  Ronald L. Davis,et al.  Molecular biology and anatomy of Drosophila olfactory associative learning , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[15]  Peter Mombaerts,et al.  How smell develops , 2001, Nature Neuroscience.

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

[17]  J. Kauer Response patterns of amphibian olfactory bulb neurones to odour stimulation , 1974, The Journal of physiology.

[18]  Desmond J. Higham,et al.  A Survey of the Explicit Runge-Kutta Method , 1995 .

[19]  N. Strausfeld,et al.  Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies , 1999, The Journal of comparative neurology.

[20]  M. Srinivasan,et al.  The concepts of ‘sameness’ and ‘difference’ in an insect , 2001, Nature.

[21]  N. Strausfeld,et al.  Taurine‐, aspartate‐ and glutamate‐like immunoreactivity identifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body , 2001, The Journal of comparative neurology.

[22]  R Huerta,et al.  Dynamical encoding by networks of competing neuron groups: winnerless competition. , 2001, Physical review letters.

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

[24]  H. Honegger,et al.  Glutamate‐like immunoreactivity marks compartments of the mushroom bodies in the brain of the cricket , 2000, The Journal of comparative neurology.

[25]  Makoto Mizunami,et al.  Function-specific distribution patterns of axon terminals of input neurons in the calyces of the mushroom body of the cockroach, Periplaneta americana , 1998, Neuroscience Letters.

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

[27]  M. Elphick,et al.  New Techniques for Whole-mount NADPH-diaphorase Histochemistry Demonstrated in Insect Ganglia , 2003, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[28]  E. A. Davidson,et al.  Learning from a fly ’ s memory , 2001 .

[29]  N. Strausfeld,et al.  The mushroom bodies of Drosophila melanogaster: An immunocytological and golgi study of Kenyon cell organization in the calyces and lobes , 2003, Microscopy research and technique.

[30]  N. Strausfeld,et al.  Parallel organization in honey bee mushroom bodies by peptidergic kenyon cells , 2000, The Journal of comparative neurology.

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

[32]  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.

[33]  I. Rodriguez,et al.  Variable Patterns of Axonal Projections of Sensory Neurons in the Mouse Vomeronasal System , 1999, Cell.

[34]  Linda B. Buck,et al.  Genetic tracing reveals a stereotyped sensory map in the olfactory cortex , 2001, Nature.

[35]  R. Traub,et al.  Neuronal Networks of the Hippocampus , 1991 .

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

[37]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

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

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

[40]  P. Mobbs The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies , 1982 .

[41]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Their participation in place memory , 1998, The Journal of comparative neurology.

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

[43]  N. Strausfeld,et al.  Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation , 2001, The Journal of comparative neurology.

[44]  David Golomb,et al.  The Number of Synaptic Inputs and the Synchrony of Large, Sparse Neuronal Networks , 2000, Neural Computation.

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

[46]  W. Gronenberg Subdivisions of hymenopteran mushroom body calyces by their afferent supply , 2001, The Journal of comparative neurology.

[47]  M. Halpern The organization and function of the vomeronasal system. , 1987, Annual review of neuroscience.

[48]  M. I. Rabinovich,et al.  Dynamical coding of sensory information with competitive networks , 2000, Journal of Physiology-Paris.

[49]  M Ennis,et al.  Functional organization of olfactory system. , 1996, Journal of neurobiology.

[50]  M. Mizunami,et al.  Topography of four classes of kenyon cells in the mushroom bodies of the cockroach , 1998, The Journal of comparative neurology.

[51]  R. Nicoll,et al.  A physiological role for GABAB receptors in the central nervous system , 1988, Nature.

[52]  N. Strausfeld,et al.  Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies , 1999, The Journal of comparative neurology.

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

[54]  B. Grünewald,et al.  Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera , 1999, The Journal of comparative neurology.

[55]  Yoshihiro Yoshihara,et al.  Molecular recognition and olfactory processing in the mammalian olfactory system , 1995, Progress in Neurobiology.

[56]  Christiane Linster,et al.  Odor Processing in the Bee: A Preliminary Study of the Role of Central Input to the Antennal Lobe , 1993, NIPS.

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

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

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

[60]  N. Strausfeld Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes , 2002, The Journal of comparative neurology.

[61]  M. Mizunami,et al.  Topography of modular subunits in the mushroom bodies of the cockroach , 1998, The Journal of comparative neurology.

[62]  P. Mombaerts,et al.  Molecular biology of odorant receptors in vertebrates. , 1999, Annual review of neuroscience.

[63]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[64]  P. Mombaerts Seven-transmembrane proteins as odorant and chemosensory receptors. , 1999, Science.

[65]  J. Hildebrand,et al.  Insect Olfaction , 1999, Springer Berlin Heidelberg.

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

[67]  G. Laurent Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[68]  M. Mizunami,et al.  Classical Olfactory Conditioning in the Cockroach Periplaneta americana , 2003, Zoological science.

[69]  N. Strausfeld,et al.  Evolution, discovery, and interpretations of arthropod mushroom bodies. , 1998, Learning & memory.

[70]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[71]  Michael Meredith Neural circuit computation: Complex patterns in the olfactory bulb , 1992, Brain Research Bulletin.

[72]  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.

[73]  M. J. Weiss Structural patterns in the corpora pedunculata of orthoptera: A reduced silver analysis , 1981, The Journal of comparative neurology.

[74]  D. Vowles The Structure and Connexions of the Corpora Pedunculata in Bees and Ants , 1955 .

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

[76]  M. Heisenberg What do the mushroom bodies do for the insect brain? an introduction. , 1998, Learning & memory.

[77]  G. Shepherd,et al.  Analysis of the onset phase of olfactory bulb unit responses to odour pulses in the salamander , 1977, The Journal of physiology.

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

[79]  T. Shibuya,et al.  Single unit responses of olfactory receptors in vultures , 1967 .

[80]  John G Hildebrand,et al.  Olfactory systems: common design, uncommon origins? , 1999, Current Opinion in Neurobiology.