In-situ recording of ionic currents in projection neurons and Kenyon cells in the olfactory pathway of the honeybee

The honeybee olfactory pathway comprises an intriguing pattern of convergence and divergence: ~60.000 olfactory sensory neurons (OSN) convey olfactory information on ~900 projection neurons (PN) in the antennal lobe (AL). To transmit this information reliably, PNs employ relatively high spiking frequencies with complex patterns. PNs project via a dual olfactory pathway to the mushroom bodies (MB). This pathway comprises the medial (m-ALT) and the lateral antennal lobe tract (l-ALT). PNs from both tracts transmit information from a wide range of similar odors, but with distinct differences in coding properties. In the MBs, PNs form synapses with many Kenyon cells (KC) that encode odors in a spatially and temporally sparse way. The transformation from complex information coding to sparse coding is a well-known phenomenon in insect olfactory coding. Intrinsic neuronal properties as well as GABAergic inhibition are thought to contribute to this change in odor representation. In the present study, we identified intrinsic neuronal properties promoting coding differences between PNs and KCs using in-situ patch-clamp recordings in the intact brain. We found very prominent K+ currents in KCs clearly differing from the PN currents. This suggests that odor coding differences between PNs and KCs may be caused by differences in their specific ion channel properties. Comparison of ionic currents of m- and l-ALT PNs did not reveal any differences at a qualitative level.

[1]  D. A. Baxter,et al.  Current- and voltage-clamp recordings and computer simulations of Kenyon cells in the honeybee. , 2004, Journal of neurophysiology.

[2]  F. Grolleau,et al.  Transient Na+-activated K+ current in beating pacemaker-isolated adult insect neurosecretory cells (dum neurones) , 1994, Neuroscience Letters.

[3]  Alexander Borst,et al.  Peptidergic counter-regulation of Ca(2+)- and Na(+)-dependent K(+) currents modulates the shape of action potentials in neurosecretory insect neurons. , 2006, Journal of neurophysiology.

[4]  M. Eckert,et al.  The large conductance Ca2+‐activated potassium channel (pSlo) of the cockroach Periplaneta americana: structure, localization in neurons and electrophysiology , 2003, The European journal of neuroscience.

[5]  F. Grolleau,et al.  Dorsal unpaired median neurones in the insect central nervous system: towards a better understanding of the ionic mechanisms underlying spontaneous electrical activity. , 2000, The Journal of experimental biology.

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

[7]  Heike S. Demmer,et al.  Intrinsic membrane properties and inhibitory synaptic input of kenyon cells as mechanisms for sparse coding? , 2009, Journal of neurophysiology.

[8]  Martin Giurfa,et al.  Differential coding by two olfactory subsystems in the honeybee brain. , 2012, Journal of neurophysiology.

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

[10]  R. Menzel,et al.  Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of the alpha‐lobe , 1993, The Journal of comparative neurology.

[11]  M. Giurfa,et al.  Differential Combinatorial Coding of Pheromones in Two Olfactory Subsystems of the Honey Bee Brain , 2015, The Journal of Neuroscience.

[12]  R. Menzel,et al.  Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. , 2002, Journal of Comparative Physiology A.

[13]  B. Grünewald,et al.  Differential expression of voltage-sensitive K+ and Ca2+ currents in neurons of the honeybee olfactory pathway , 2003, Journal of Experimental Biology.

[14]  Dagoberto Tapia,et al.  Different Corticostriatal Integration in Spiny Projection Neurons from Direct and Indirect Pathways , 2010, Front. Syst. Neurosci..

[15]  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.

[16]  R. Menzel,et al.  Effect of GABAergic inhibition on odorant concentration coding in mushroom body intrinsic neurons of the honeybee , 2014, Journal of Comparative Physiology A.

[17]  Geraldine A. Wright,et al.  Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees , 2013, Nature Communications.

[18]  C. G. Perk,et al.  Dopamine modulation of honey bee (Apis mellifera) antennal-lobe neurons. , 2006, Journal of neurophysiology.

[19]  P. Roche,et al.  Macropinocytosis in phagocytes: regulation of MHC class-II-restricted antigen presentation in dendritic cells , 2015, Front. Physiol..

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

[21]  R Menzel,et al.  IA in Kenyon cells of the mushroom body of honeybees resembles shaker currents: kinetics, modulation by K+, and simulation. , 1999, Journal of neurophysiology.

[22]  R. Mostafa,et al.  Suicidal Ideation Is Associated with Altered Variability of Fingertip Photo-Plethysmogram Signal in Depressed Patients , 2017, Front. Physiol..

[23]  P. Kloppenburg,et al.  Properties and physiological function of Ca2+-dependent K+ currents in uniglomerular olfactory projection neurons. , 2016, Journal of neurophysiology.

[24]  J. Dubnau.  Ode to the Mushroom Bodies , 2012, Science.

[25]  Olfactory subsystems in the honeybee: sensory supply and sex specificity , 2014, Cell and Tissue Research.

[26]  R. Menzel,et al.  Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. , 2005, Journal of neurophysiology.

[27]  M. Stopfer,et al.  Dye fills reveal additional olfactory tracts in the protocerebrum of wild‐type Drosophila , 2012, The Journal of comparative neurology.

[28]  P. Sah,et al.  Channels underlying neuronal calcium-activated potassium currents , 2002, Progress in Neurobiology.

[29]  Jeffrey A. Riffell,et al.  Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance , 2009, Journal of biology.

[30]  Julie H. Simpson,et al.  A Systematic Nomenclature for the Insect Brain , 2014, Neuron.

[31]  Wolfgang Rössler,et al.  Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Anneke Meyer,et al.  It takes two—coincidence coding within the dual olfactory pathway of the honeybee , 2015, Front. Physiol..

[33]  M. Palmer,et al.  Honeybee Kenyon cells are regulated by a tonic GABA receptor conductance. , 2014, Journal of neurophysiology.

[34]  Johannes Esslen,et al.  Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.) , 1976, Zoomorphologie.

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

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

[37]  Hans-Christian Hege,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

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

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

[40]  Mark Stopfer,et al.  Insect olfactory coding and memory at multiple timescales , 2011, Current Opinion in Neurobiology.

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

[42]  Aaditya V. Rangan,et al.  Intrinsic and Network Mechanisms Constrain Neural Synchrony in the Moth Antennal Lobe , 2016, Front. Physiol..

[43]  Sebastian Kirschner,et al.  Dual olfactory pathway in the honeybee, Apis mellifera , 2006, The Journal of comparative neurology.

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

[45]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[46]  Menzel,et al.  The role of glomeruli in the neural representation of odours: results from optical recording studies. , 2001, Journal of insect physiology.

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

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

[49]  Sreekanth H. Chalasani,et al.  Olfactory networks: from sensation to perception. , 2011, Current opinion in genetics & development.

[50]  R. Menzel,et al.  Optical imaging of concealed brain activity using a gold mirror in honeybees. , 2012, Journal of insect physiology.

[51]  Andrew C. Lin,et al.  Sparse, Decorrelated Odor Coding in the Mushroom Body Enhances Learned Odor Discrimination , 2014, Nature Neuroscience.

[52]  R Menzel,et al.  Ionic currents of Kenyon cells from the mushroom body of the honeybee , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  P. Sah,et al.  Small-conductance Ca2+-activated K+ channels: form and function. , 2012, Annual review of physiology.