Higher order visual input to the mushroom bodies in the bee, Bombus impatiens.

To produce appropriate behaviors based on biologically relevant associations, sensory pathways conveying different modalities are integrated by higher-order central brain structures, such as insect mushroom bodies. To address this function of sensory integration, we characterized the structure and response of optic lobe (OL) neurons projecting to the calyces of the mushroom bodies in bees. Bees are well known for their visual learning and memory capabilities and their brains possess major direct visual input from the optic lobes to the mushroom bodies. To functionally characterize these visual inputs to the mushroom bodies, we recorded intracellularly from neurons in bumblebees (Apidae: Bombus impatiens) and a single neuron in a honeybee (Apidae: Apis mellifera) while presenting color and motion stimuli. All of the mushroom body input neurons were color sensitive while a subset was motion sensitive. Additionally, most of the mushroom body input neurons would respond to the first, but not to subsequent, presentations of repeated stimuli. In general, the medulla or lobula neurons projecting to the calyx signaled specific chromatic, temporal, and motion features of the visual world to the mushroom bodies, which included sensory information required for the biologically relevant associations bees form during foraging tasks.

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

[2]  R. Menzel,et al.  Chromatic properties of interneurons in the optic lobes of the bee , 2004, Journal of comparative physiology.

[3]  E. Yang,et al.  Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. , 2004, Journal of insect physiology.

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

[5]  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.

[6]  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.

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

[8]  Wulfila Gronenberg,et al.  Brain Allometry in Bumblebee and Honey Bee Workers , 2005, Brain, Behavior and Evolution.

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

[10]  Randolf Menzel,et al.  Neurobiology and Behavior of Honeybees , 1987, Springer Berlin Heidelberg.

[11]  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.

[12]  H. Hertel,et al.  The Physiology and Morphology of Centrally Projecting Visual Interneurones in the Honeybee Brain , 1987 .

[13]  Randolf Menzel,et al.  Color Vision in Honeybees: Metric, Dimensions, Constancy, and Ecological Aspects , 1987 .

[14]  R. Reid,et al.  Precise Firing Events Are Conserved across Neurons , 2002, The Journal of Neuroscience.

[15]  G. Laurent,et al.  Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts , 2007, Nature.

[16]  T. Schultz,et al.  Evidence for the origin of eusociality in the corbiculate bees (Hymenoptera: Apidae) , 2001 .

[17]  H. Honegger,et al.  Cobalt sulphide staining of optic fibres in the brain of the cricket, Gryllus campestris , 1975, Cell and Tissue Research.

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

[19]  W. Gronenberg Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain , 1986 .

[20]  G. E. Gregory The Bodian Protargol Technique , 1980 .

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

[22]  Wulfila Gronenberg,et al.  Electrical Potentials Indicate Stimulus Expectancy in the Brains of Ants and Bees , 2005, Cellular and Molecular Neurobiology.

[23]  M. Giurfa Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well , 2007, Journal of Comparative Physiology A.

[24]  B. Swinderen,et al.  Attention-like processes in Drosophila require short-term memory genes. , 2007 .

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

[26]  C. Rowell,et al.  The orthopteran descending movement detector (DMD) neurones: a characterisation and review , 1971, Zeitschrift für vergleichende Physiologie.

[27]  T. Shimozawa Response entrainment of movement fibers in the optic tract of crayfish , 1975, Biological Cybernetics.

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

[29]  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.

[30]  N. Strausfeld,et al.  Visual Motion-Detection Circuits in Flies: Parallel Direction- and Non-Direction-Sensitive Pathways between the Medulla and Lobula Plate , 1996, The Journal of Neuroscience.

[31]  Li Liu,et al.  Context generalization in Drosophila visual learning requires the mushroom bodies , 1999, Nature.

[32]  A. Straw,et al.  A `bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity , 2006, Journal of Experimental Biology.

[33]  R. Menzel,et al.  Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain , 2005, Journal of Experimental Biology.

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

[35]  U. Homberg Processing of antennal information in extrinsic mushroom body neurons of the bee brain , 1984, Journal of Comparative Physiology A.

[36]  R. Menzel,et al.  Chromatic properties of interneurons in the optic lobes of the bee , 1977, Journal of comparative physiology.

[37]  B. Tabashnik,et al.  Development time and resistance to Bt crops , 1999, Nature.

[38]  W. Gronenberg,et al.  Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera) , 2002, The Journal of comparative neurology.

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

[40]  W. Ribi,et al.  The second and third optic ganglia of the worker bee , 1981, Cell and Tissue Research.

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

[42]  Randolf Menzel,et al.  Dimensions of cognition in an insect, the honeybee. , 2006, Behavioral and cognitive neuroscience reviews.

[43]  Shaowu Zhang,et al.  PROBING PERCEPTION IN A MINIATURE BRAIN : PATTERN RECOGNITION AND MAZE NAVIGATION IN HONEYBEES , 1998 .

[44]  H. Hertel,et al.  The physiology and morphology of visual commissures in the honeybee brain , 1987 .

[45]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[46]  R. Menzel,et al.  A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal‐calycal tract , 2003, The Journal of comparative neurology.

[47]  Cole Gilbert,et al.  Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata , 1991, Journal of Comparative Physiology A.

[48]  N. Strausfeld,et al.  Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana , 1997, The Journal of comparative neurology.

[49]  Tamar Keasar,et al.  Location and Color Learning in Bumblebees in a Two-Phase Conditioning Experiment , 2001, Journal of Insect Behavior.

[50]  P. Mobbs Neural networks in the mushroom bodies of the honeybee , 1984 .

[51]  F. Baumann,et al.  A depolarizing aftereffect of intense light in the drone visual receptor. , 1972, Vision research.

[52]  R. Menzel,et al.  The spectral input systems of hymenopteran insects and their receptor-based colour vision , 2004, Journal of Comparative Physiology A.

[53]  M. Srinivasan Pattern recognition in the honeybee: Recent progress , 1994 .

[54]  H. Hertel Chromatic properties of identified interneurons in the optic lobes of the bee , 1980, Journal of comparative physiology.

[55]  R. Menzel Memory dynamics in the honeybee , 1999, Journal of Comparative Physiology A.