Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee Apis mellifera

SUMMARY Honeybees learn to associate an odor with sucrose reward under conditions that allow the monitoring of neural activity by imaging Ca2+ transients in morphologically identified neurons. Here we report such recordings from mushroom body extrinsic neurons – which belong to a recurrent tract connecting the output of the mushroom body with its input, potentially providing inhibitory feedback – and other extrinsic neurons. The neurons' responses to the learned odor and two novel control odors were measured 24 h after learning. We found that calcium responses to the learned odor and an odor that was strongly generalized with it were enhanced compared with responses to a weakly generalized control. Thus, the physiological responses measured in these extrinsic neurons accurately reflect what is observed in behavior. We conclude that the recorded recurrent neurons feed information back to the mushroom body about the features of learned odor stimuli. Other extrinsic neurons may signal information about learned odors to different brain regions.

[1]  R. Menzel,et al.  Mushroom Body Output Neurons Encode Odor–Reward Associations , 2011, The Journal of Neuroscience.

[2]  R. Menzel,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[3]  Ronald L. Davis,et al.  A Late-Phase, Long-Term Memory Trace Forms in the γ Neurons of Drosophila Mushroom Bodies after Olfactory Classical Conditioning , 2010, The Journal of Neuroscience.

[4]  A. Irintchev,et al.  Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus. , 2010, Cerebral cortex.

[5]  Randolf Menzel,et al.  Differential Odor Processing in Two Olfactory Pathways in the Honeybee , 2009, Front. Syst. Neurosci..

[6]  J. Dupuis,et al.  Glutamatergic and GABAergic effects of fipronil on olfactory learning and memory in the honeybee , 2009, Invertebrate Neuroscience.

[7]  R. Menzel,et al.  In vivo Ca2+ imaging of mushroom body neurons during olfactory learning in the honey bee. , 2009, Journal of visualized experiments : JoVE.

[8]  Peter K. Dearden,et al.  The honeybee Apis mellifera. , 2009, Cold Spring Harbor protocols.

[9]  Ronald L. Davis,et al.  The GABAA Receptor RDL Suppresses the Conditioned Stimulus Pathway for Olfactory Learning , 2009, The Journal of Neuroscience.

[10]  Ronald L. Davis,et al.  The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning , 2008, Nature Neuroscience.

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

[12]  W. Rössler,et al.  Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. , 2008, Arthropod structure & development.

[13]  M. Giurfa,et al.  Inhibitory neurotransmission and olfactory memory in honeybees , 2008, Neurobiology of Learning and Memory.

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

[15]  R. Menzel,et al.  Associative and Non-Associative Plasticity in Kenyon Cells of the Honeybee Mushroom Body , 2008, Frontiers in systems neuroscience.

[16]  Glenn C. Turner,et al.  Olfactory representations by Drosophila mushroom body neurons. , 2008, Journal of neurophysiology.

[17]  Ronald L. Davis,et al.  GABAA Receptor RDL Inhibits Drosophila Olfactory Associative Learning , 2007, Neuron.

[18]  R. Menzel,et al.  Learning-Related Plasticity in PE1 and Other Mushroom Body-Extrinsic Neurons in the Honeybee Brain , 2007, The Journal of Neuroscience.

[19]  Gisbert Schneider,et al.  Predicting olfactory receptor neuron responses from odorant structure , 2007, Chemistry Central journal.

[20]  Ronald L. Davis,et al.  Drosophila α/β Mushroom Body Neurons Form a Branch-Specific, Long-Term Cellular Memory Trace after Spaced Olfactory Conditioning , 2006, Neuron.

[21]  R. Menzel,et al.  Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons , 2006, Journal of Comparative Physiology A.

[22]  Ronald L. Davis,et al.  Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. , 2006, Neuron.

[23]  Ronald L. Davis,et al.  Drosophila DPM Neurons Form a Delayed and Branch-Specific Memory Trace after Olfactory Classical Conditioning , 2005, Cell.

[24]  R. Menzel,et al.  Three‐dimensional average‐shape atlas of the honeybee brain and its applications , 2005, The Journal of comparative neurology.

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

[26]  M. Dacher,et al.  Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera) , 2005, Pharmacology Biochemistry and Behavior.

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

[28]  Ton Bisseling,et al.  Biology by Numbers—Introducing Quantitation into Life Science Education , 2005, PLoS biology.

[29]  B. Smith,et al.  Variation in complex olfactory stimuli and its influence on odour recognition , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  B. Smith,et al.  Ability of Honeybee, Apis mellifera, to Detect and Discriminate Odors of Varieties of Canola (Brassica rapa and Brassica napus) and Snapdragon Flowers (Antirrhinum majus) , 2002, Journal of Chemical Ecology.

[31]  M. Heisenberg Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[32]  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.

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

[34]  R. Menzel,et al.  Visualizing mushroom body response to a conditioned odor in honeybees , 2001, Naturwissenschaften.

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

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

[37]  B. Grünewald,et al.  Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera , 1999, Journal of Comparative Physiology A.

[38]  S. Sachse,et al.  The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code , 1999, The European journal of neuroscience.

[39]  R. Menzel,et al.  Olfactory discrimination ability and odor structure-activity relationships in honeybees. , 1999, Chemical senses.

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

[41]  R. Menzel,et al.  Associative learning modifies neural representations of odors in the insect brain , 1999, Nature Neuroscience.

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

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

[44]  Randolf Menzel,et al.  A semi-in-vivo preparation for optical recording of the insect brain , 1997, Journal of Neuroscience Methods.

[45]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[46]  M. Hammer,et al.  Behavioral, neural and cellular components underlying olfactory learning in the honeybee , 1996, Journal of Physiology-Paris.

[47]  R. Menzel,et al.  Honey bees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory , 1996, Animal Behaviour.

[48]  R. Menzel,et al.  Learning and memory in honeybees: from behavior to neural substrates. , 1996, Annual review of neuroscience.

[49]  M. Hammer,et al.  Learning and memory in the honeybee , 1995 .

[50]  M. Hammer,et al.  Learning and memory in the honeybee. , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[52]  M. Hammer An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[53]  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.

[54]  J. Mauelshagen,et al.  Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. , 1993, Journal of neurophysiology.

[55]  S. File BENZODIAZEPINES AND MEMORY , 1992, Clinical neuropharmacology.

[56]  V. Rehder Quantification of the honeybee's proboscis reflex by electromyographic recordings , 1987 .

[57]  T. Kingan,et al.  Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity , 1985, Brain Research.

[58]  R. Lister The amnesic action of benzodiazepines in man , 1985, Neuroscience & Biobehavioral Reviews.

[59]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

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

[61]  T. SHALLICE,et al.  Learning and Memory , 1970, Nature.

[62]  A. Calvin Olfactory Discrimination. , 1960, Science.