Evidence for absence of bilateral transfer of olfactory learned information in Apis dorsata and Apis mellifera

Capacity and condition under which lateral transfer of olfactory memory is possible in insects are still debated. Here we present evidence consistent with lack of ability to transfer olfactory associative memory in two species of honeybees, Apis mellifera and Apis dorsata in a PER associative conditioning paradigm where the untrained antenna is blocked by an insulating coat. We show that the olfactory system on each side of the bee can learn and retrieve independently and the retrieval using the antenna on the side contralateral to the trained one is not affected by the training. Recreating the paradigm in which the memory on the contralateral side has been reported at three hours after training we see that the memory is available on the contralateral side immediately after training and moreover, training with trained side antenna coated with insulator does not prevent learning, pointing to a possible insufficiency of block of odor stimuli in this paradigm. Bee does not learn the odor stimuli applied to one side alone as a stimulus different from odor presented to both sides. Moreover the behaviour of the bee as a whole can be predicted if the sides are assumed to learn and store independently and the organism as a whole is able to retrieve the memory if either of the sides have learned. Summary Statement The two halves of honeybee brain store and retrieve olfactory associative memories independently.

[1]  Rüdiger Wehner,et al.  Information Processing in the Visual Systems of Anthropods , 1972, Springer Berlin Heidelberg.

[2]  R. Menzel,et al.  Learning Experiments on the Use of Side — Specific Information in the Olfactory and Visual System in the Honey Bee (Apis mellifica) , 1972 .

[3]  R. Menzel,et al.  Localization of short‐term memory in the brain of the bee, Apis mellifera , 1980 .

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

[5]  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.

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

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

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

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

[10]  M. Hammer.  The neural basis of associative reward learning in honeybees , 1997, Trends in Neurosciences.

[11]  M. Gazzaniga.  Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? , 2000, Brain : a journal of neurology.

[12]  R. Menzel,et al.  Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. , 2001, Learning & memory.

[13]  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.

[14]  M. Giurfa,et al.  Hydroxyurea-induced partial mushroom body ablation in the honeybee Apis mellifera: volumetric analysis and quantitative protein determination. , 2002, Journal of neurobiology.

[15]  M. Hammer,et al.  Side-specificity of olfactory learning in the honeybee: US input side. , 2002, Learning & memory.

[16]  B. Gerber,et al.  Hydroxyurea-induced partial mushroom body ablation does not affect acquisition and retention of olfactory differential conditioning in honeybees. , 2002, Journal of neurobiology.

[17]  R. Menzel,et al.  Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes , 2003, Neuroscience.

[18]  F. Aboitiz,et al.  One hundred million years of interhemispheric communication: the history of the corpus callosum. , 2003, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[19]  J. Royet,et al.  Lateralization of olfactory processes. , 2004, Chemical senses.

[20]  M. Giurfa,et al.  Partial unilateral lesions of the mushroom bodies affect olfactory learning in honeybees Apis mellifera L. , 2005, The European journal of neuroscience.

[21]  M. Srinivasan,et al.  Lateralization of Olfaction in the Honeybee Apis mellifera , 2006, Current Biology.

[22]  G. Vallortigara.  The evolutionary psychology of left and right: costs and benefits of lateralization. , 2006, Developmental psychobiology.

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

[24]  R. Mihrshahi.  The corpus callosum as an evolutionary innovation. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

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

[26]  S. Ghirlanda,et al.  Intraspecific competition and coordination in the evolution of lateralization , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  M. Corballis.  The evolution and genetics of cerebral asymmetry , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  J. Carlson,et al.  Olfactory Perception: Receptors, Cells, and Circuits , 2009, Cell.

[29]  J. Sanes,et al.  Design Principles of Insect and Vertebrate Visual Systems , 2010, Neuron.

[30]  U. Kaupp.  Olfactory signalling in vertebrates and insects: differences and commonalities , 2010, Nature Reviews Neuroscience.

[31]  G. Vallortigara,et al.  Lateralization in the Invertebrate Brain: Left-Right Asymmetry of Olfaction in Bumble Bee, Bombus terrestris , 2011, PloS one.

[32]  B. Hansson,et al.  Evolution of Insect Olfaction , 2011, Neuron.

[33]  A multimodal approach for tracing lateralisation along the olfactory pathway in the honeybee through electrophysiological recordings, morpho-functional imaging, and behavioural studies , 2011, European Biophysics Journal.

[34]  R. Menzel,et al.  Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: A step toward standardized procedures , 2012, Journal of Neuroscience Methods.

[35]  R. Menzel.  The honeybee as a model for understanding the basis of cognition , 2012, Nature Reviews Neuroscience.

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

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

[38]  M. D. Lussanet,et al.  An ancestral axial twist explains the contralateral forebrain and the optic chiasm in vertebrates , 2010, 1003.1872.

[39]  R. Menzel.  Chapter 29 – In Search of the Engram in the Honeybee Brain , 2013 .

[40]  E. Frasnelli.  Brain and behavioral lateralization in invertebrates , 2013, Front. Psychol..

[41]  B. Smith,et al.  Octopamine modulates activity of neural networks in the honey bee antennal lobe , 2013, Journal of Comparative Physiology A.

[42]  L. Richards,et al.  Evolution and development of interhemispheric connections in the vertebrate forebrain , 2014, Front. Hum. Neurosci..

[43]  G. Vallortigara,et al.  The Bee as a Model to Investigate Brain and Behavioural Asymmetries , 2014, Insects.

[44]  M. Gazzaniga.  The split-brain: Rooting consciousness in biology , 2014, Proceedings of the National Academy of Sciences.

[45]  Runsheng Chen,et al.  Lateralization of gene expression in the honeybee brain during olfactory learning , 2016, Scientific Reports.

[46]  R. Menzel,et al.  Neural correlates of side-specific odour memory in mushroom body output neurons , 2016, Proceedings of the Royal Society B: Biological Sciences.

[47]  Colin Klein,et al.  What insects can tell us about the origins of consciousness , 2016, Proceedings of the National Academy of Sciences.

[48]  M. Corballis.  The Evolution of Lateralized Brain Circuits , 2017, Front. Psychol..

[49]  Lars Chittka,et al.  Insect Bio-inspired Neural Network Provides New Evidence on How Simple Feature Detectors Can Enable Complex Visual Generalization and Stimulus Location Invariance in the Miniature Brain of Honeybees , 2017, PLoS Comput. Biol..

[50]  Joby Joseph,et al.  Evolutionarily conserved anatomical and physiological properties of olfactory pathway till fourth order neurons in a species of grasshopper (Hieroglyphus banian) , 2018, bioRxiv.

[51]  Joby Joseph,et al.  Characterization of the olfactory system in Apis dorsata, an Asian honey bee , 2018, bioRxiv.