Local interneurons and projection neurons in the antennal lobe from a spiking point of view.

Local computation in microcircuits is an essential feature of distributed information processing in vertebrate and invertebrate brains. The insect antennal lobe represents a spatially confined local network that processes high-dimensional and redundant peripheral input to compute an efficient odor code. Social insects can rely on a particularly rich olfactory receptor repertoire, and they exhibit complex odor-guided behaviors. This corresponds with a high anatomical complexity of their antennal lobe network. In the honeybee, a large number of glomeruli that receive sensory input are interconnected by a dense network of local interneurons (LNs). Uniglomerular projection neurons (PNs) integrate sensory and recurrent local network input into an efficient spatio-temporal odor code. To investigate the specific computational roles of LNs and PNs, we measured several features of sub- and suprathreshold single-cell responses to in vivo odor stimulation. Using a semisupervised cluster analysis, we identified a combination of five characteristic features as sufficient to separate LNs and PNs from each other, independent of the applied odor-stimuli. The two clusters differed significantly in all these five features. PNs showed a higher spontaneous subthreshold activation, assumed higher peak response rates and a more regular spiking pattern. LNs reacted considerably faster to the onset of a stimulus, and their responses were more reliable across stimulus repetitions. We discuss possible mechanisms that can explain our results, and we interpret cell-type-specific characteristics with respect to their functional relevance.

[1]  Brian H. Smith,et al.  Ensemble Response in Mushroom Body Output Neurons of the Honey Bee Outpaces Spatiotemporal Odor Processing Two Synapses Earlier in the Antennal Lobe , 2012, PloS one.

[2]  P. Streit,et al.  Distribution of GABA-like immunoreactivity in the pigeon brain , 1988, Neuroscience.

[3]  C. Galizia,et al.  Allatostatin immunoreactivity in the honeybee brain , 2010, The Journal of comparative neurology.

[4]  B. Kimmerle,et al.  Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy , 2003, Journal of Comparative Physiology A.

[5]  M. Nawrot Dynamics of sensory processing in the dual olfactory pathway of the honeybee , 2012, Apidologie.

[6]  Prasad Gabbur,et al.  Spiking Patterns and Their Functional Implications in the Antennal Lobe of the Tobacco Hornworm Manduca sexta , 2011, PloS one.

[7]  Reinhard F. Stocker,et al.  The organization of the chemosensory system in Drosophila melanogaster: a rewiew , 2004, Cell and Tissue Research.

[8]  D. Malun Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double-labeling electron microscopic study , 2004, Histochemistry.

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

[10]  Jürgen Rybak,et al.  The Digital Honey Bee Brain Atlas , 2012 .

[11]  Adrián Ponce-Alvarez,et al.  Comparison of local measures of spike time irregularity and relating variability to firing rate in motor cortical neurons , 2010, Journal of Computational Neuroscience.

[12]  W. Witthöft,et al.  Absolute anzahl und verteilung der zellen im him der honigbiene , 2004, Zeitschrift für Morphologie der Tiere.

[13]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[14]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

[15]  Shawn R. Olsen,et al.  Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila , 2008, Trends in Neurosciences.

[16]  Silke Sachse,et al.  The coding of odour‐intensity in the honeybee antennal lobe: local computation optimizes odour representation , 2003, The European journal of neuroscience.

[17]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[18]  B. Matthews Comparison of the predicted and observed secondary structure of T4 phage lysozyme. , 1975, Biochimica et biophysica acta.

[19]  R. Stocker,et al.  Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. , 1997, Journal of neurobiology.

[20]  J. Hildebrand,et al.  Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta , 1993, Journal of Comparative Physiology A.

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

[22]  J. Hildebrand,et al.  Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta , 1988, Cell and Tissue Research.

[23]  W. Rössler,et al.  Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies. , 2011, Arthropod structure & development.

[24]  Jeffrey A. Riffell,et al.  The neurobiology of insect olfaction: Sensory processing in a comparative context , 2011, Progress in Neurobiology.

[25]  Randolf Menzel,et al.  Rapid odor processing in the honeybee antennal lobe network , 2009 .

[26]  C. Galizia,et al.  Elemental and configural olfactory coding by antennal lobe neurons of the honeybee (Apis mellifera) , 2011, Journal of Comparative Physiology A.

[27]  Andreas T. Schaefer,et al.  Maintaining Accuracy at the Expense of Speed Stimulus Similarity Defines Odor Discrimination Time in Mice , 2004, Neuron.

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

[29]  C Giovanni Galizia,et al.  Parallel olfactory systems in insects: anatomy and function. , 2010, Annual review of entomology.

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

[31]  Silke Sachse,et al.  Topography and Dynamics of the Olfactory System , 2006 .

[32]  W. Rössler,et al.  Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf‐cutting ant workers (A. vollenweideri) , 2010, Developmental neurobiology.

[33]  Shawn R. Olsen,et al.  Lateral presynaptic inhibition mediates gain control in an olfactory circuit , 2008, Nature.

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

[35]  P. Distler,et al.  Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. uniglomerular projection neurons , 1997, The Journal of comparative neurology.

[36]  Zbynek Bures The stochastic properties of input spike trains control neuronal arithmetic , 2012, Biological Cybernetics.

[37]  Anneke Meyer Characterisation of Local Interneurons in the Antennal Lobe of the Honeybee , 2011 .

[38]  U. Homberg,et al.  Neuropeptides in interneurons of the insect brain , 2006, Cell and Tissue Research.

[39]  Stefan Rotter,et al.  Measurement of variability dynamics in cortical spike trains , 2008, Journal of Neuroscience Methods.

[40]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[41]  Katherine I. Nagel,et al.  Biophysical mechanisms underlying olfactory receptor neuron dynamics , 2010, Nature Neuroscience.

[42]  Jeffrey A. Riffell,et al.  Characterization and Coding of Behaviorally Significant Odor Mixtures , 2009, Current Biology.

[43]  E. Parzen On Estimation of a Probability Density Function and Mode , 1962 .

[44]  Martin P. Nawrot,et al.  Analysis and Interpretation of Interval and Count Variability in Neural Spike Trains , 2010 .

[45]  B. Strowbridge Linking Local Circuit Inhibition to Olfactory Behavior: A Critical Role for Granule Cells in Olfactory Discrimination , 2010, Neuron.

[46]  S. Sachse,et al.  Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. , 2002, Journal of neurophysiology.

[47]  David Harel,et al.  A metric for odorant comparison , 2008, Nature Methods.

[48]  Wei Zhang,et al.  Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway , 2010, Proceedings of the National Academy of Sciences.

[49]  A. Savitzky,et al.  Smoothing and Differentiation of Data by Simplified Least Squares Procedures. , 1964 .

[50]  Martin F. Brill,et al.  Parallel processing in the honeybee olfactory pathway: structure, function, and evolution , 2013, Journal of Comparative Physiology A.

[51]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[52]  R. Kanzaki,et al.  Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori , 2008, The Journal of comparative neurology.

[53]  Wolfgang Rössler,et al.  Caste- and sex-specific adaptations within the olfactory pathway in the brain of the ant Camponotus floridanus. , 2008, Arthropod structure & development.

[54]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[55]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[56]  A. Borst,et al.  Neuronal architecture of the antennal lobe in Drosophila melanogaster , 1990, Cell and Tissue Research.

[57]  Gisbert Schneider,et al.  Processing and classification of chemical data inspired by insect olfaction , 2007, Proceedings of the National Academy of Sciences.

[58]  G. Bicker,et al.  Distribution of GABA‐like immunoreactivity in the brain of the honeybee , 1986, The Journal of comparative neurology.

[59]  X. Sun,et al.  Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours , 1993 .

[60]  A. Husch,et al.  Distinct electrophysiological properties in subtypes of nonspiking olfactory local interneurons correlate with their cell type-specific Ca2+ current profiles. , 2009, Journal of neurophysiology.

[61]  R. A. Hensbroek,et al.  Spontaneous Activity Signatures of Morphologically Identified Interneurons in the Vestibulocerebellum , 2011, The Journal of Neuroscience.

[62]  G Laurent,et al.  A dendritic gain control mechanism in axonless neurons of the locust, Schistocerca americana. , 1993, The Journal of physiology.

[63]  Alan Carleton,et al.  Dynamic Ensemble Odor Coding in the Mammalian Olfactory Bulb: Sensory Information at Different Timescales , 2008, Neuron.

[64]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[65]  Stefan Rotter,et al.  Single-trial estimation of neuronal firing rates: From single-neuron spike trains to population activity , 1999, Journal of Neuroscience Methods.

[66]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.

[67]  Mark Stopfer,et al.  Spontaneous Olfactory Receptor Neuron Activity Determines Follower Cell Response Properties , 2012, The Journal of Neuroscience.

[68]  S. Sachse,et al.  Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. , 2010, Journal of neurophysiology.

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

[70]  M. Giurfa,et al.  Perceptual and Neural Olfactory Similarity in Honeybees , 2005, PLoS biology.

[71]  Vreeswijk,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 2010 .

[72]  Daniel Flanagan,et al.  Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybeeApis mellifera , 1989, Journal of Comparative Physiology A.

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

[74]  Martin P. Nawrot,et al.  Parallel Processing via a Dual Olfactory Pathway in the Honeybee , 2013, The Journal of Neuroscience.

[75]  Christophe Pouzat,et al.  Improved spike-sorting by modeling firing statistics and burst-dependent spike amplitude attenuation: a Markov chain Monte Carlo approach. , 2004, Journal of neurophysiology.

[76]  Karl Pearson F.R.S. LIII. On lines and planes of closest fit to systems of points in space , 1901 .

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

[78]  Uwe Homberg,et al.  Antennal Lobe Structure , 1999 .

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

[80]  Stefan Rotter,et al.  Elimination of response latency variability in neuronal spike trains , 2003, Biological Cybernetics.

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

[82]  S. Grillner,et al.  Microcircuits : the interface between neurons and global brain function , 2006 .

[83]  Andreas Husch,et al.  Differences of Ca2+ handling properties in identified central olfactory neurons of the antennal lobe. , 2009, Cell calcium.

[84]  R. Chapman,et al.  Phenotypic plasticity in numbers of antennal chemoreceptors in a grasshopper: effects of food , 1998, Journal of Comparative Physiology A.

[85]  C. Reisenman,et al.  Histamine‐immunoreactive local neurons in the antennal lobes of the hymenoptera , 2010, The Journal of comparative neurology.

[86]  Ad Aertsen,et al.  FIND - A unified framework for neural data analysis , 2008, Neural Networks.

[87]  Physiological and morphological characterization of two Bacillus strains , 2013 .

[88]  J. Sanes,et al.  Structure and development of antennae in a moth, Manduca sexta. , 1976, Developmental biology.

[89]  G. Galizia 4.41 – Insect Olfaction , 2008 .

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

[91]  B. Smith,et al.  Associative Conditioning Tunes Transient Dynamics of Early Olfactory Processing , 2009, The Journal of Neuroscience.

[92]  L. Luo,et al.  Diversity and Wiring Variability of Olfactory Local Interneurons in the Drosophila Antennal Lobe , 2010, Nature Neuroscience.