Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens)

The mechanisms of processing a visual scene involve segregating features (such as color) into separate information channels at different stages within the brain, processing these features, and then integrating this information at higher levels in the brain. To examine how this process takes place in the insect brain, we focused on the medulla, an area within the optic lobe through which all of the visual information from the retina must pass before it proceeds to central brain areas. We used histological and immunocytochemical techniques to examine the bumblebee medulla and found that the medulla is divided into eight layers. We then recorded and morphologically identified 27 neurons with processes in the medulla. During our recordings we presented color cues to determine whether response types correlated with locations of the neural branching patterns of the filled neurons among the medulla layers. Neurons in the outer medulla layers had less complex color responses compared to neurons in the inner medulla layers and there were differences in the temporal dynamics of the responses among the layers. Progressing from the outer to the inner medulla, neurons in the different layers appear to process increasingly complex aspects of the natural visual scene. J. Comp. Neurol. 513:441–456, 2009. © 2009 Wiley‐Liss, Inc.

[1]  Walter Kaiser,et al.  Horizontal movement detectors of honeybees: Directionally-selective visual neurons in the lobula and brain , 1982, Journal of comparative physiology.

[2]  Uwe Homberg,et al.  Movement‐sensitive, polarization‐sensitive, and light‐sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria , 1997, The Journal of comparative neurology.

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

[4]  Nicholas J. Strausfeld,et al.  Beneath the Compound Eye: Neuroanatomical Analysis and Physiological Correlates in the Study of Insect Vision , 1989 .

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

[6]  Angelique C Paulk,et al.  Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. , 2008, Arthropod structure & development.

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

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

[9]  F. Gribakin Cellular Basis of Colour Vision in the Honey Bee , 1969, Nature.

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

[11]  Andrew M Dacks,et al.  Phylogeny of a serotonin‐immunoreactive neuron in the primary olfactory center of the insect brain , 2006, The Journal of comparative neurology.

[12]  M. Ibbotson Evidence for velocity–tuned motion-sensitive descending neurons in the honeybee , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  N. Strausfeld,et al.  Retinotopic pathways providing motion‐selective information to the lobula from peripheral elementary motion‐detecting circuits , 2003, The Journal of comparative neurology.

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

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

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

[17]  W. Ribi The first optic ganglion of the bee , 1979, Cell and Tissue Research.

[18]  N. J. Strausfeld,et al.  The columnar organization of the second synaptic region of the visual system of Musca domestica L. , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

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

[20]  N. Strausfeld,et al.  Diverse speed response properties of motion sensitive neurons in the fly’s optic lobe , 2007, Journal of Comparative Physiology A.

[21]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure , 1989, Cell and Tissue Research.

[22]  J. Erber,et al.  The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.) , 2004, Journal of Comparative Physiology A.

[23]  Gert Stange,et al.  Directional Selectivity in the Simple Eye of an Insect , 2008, The Journal of Neuroscience.

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

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

[26]  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.

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

[28]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[29]  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.

[30]  J. Hildebrand,et al.  Histamine‐immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta , 1991, The Journal of comparative neurology.

[31]  E. Buchner,et al.  Genetic depletion of histamine from the nervous system of Drosophila eliminates specific visual and mechanosensory behavior , 1996, Journal of Comparative Physiology A.

[32]  N. Strausfeld,et al.  Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly , 1998, The Journal of comparative neurology.

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

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

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

[36]  D. Osorio,et al.  Directionally selective cells in the locust medulla , 1986, Journal of Comparative Physiology A.

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

[38]  J. Fellous,et al.  The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain , 2008, The Journal of Neuroscience.

[39]  Andrew D. Straw,et al.  Vision Egg: an Open-Source Library for Realtime Visual Stimulus Generation , 2008, Frontiers Neuroinformatics.

[40]  E. Callaway Structure and function of parallel pathways in the primate early visual system , 2005, The Journal of physiology.

[41]  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.

[42]  R. Menzel Spectral sensitivity of monopolar cells in the bee lamina , 1974, Journal of comparative physiology.

[43]  Dora Fix Ventura,et al.  Response properties of stained monopolar cells in the honeybee lamina , 1992, Journal of Comparative Physiology A.

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

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

[46]  R. Hardie Is histamine a neurotransmitter in insect photoreceptors? , 1987, Journal of Comparative Physiology A.

[47]  L. Goodman,et al.  Ocellar projections within the central nervous system of the worker honey bee, Apis mellifera , 1977, Cell and Tissue Research.

[48]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  F. Gribakin The distribution of the long wave photoreceptors in the compound eye of the honey bee as revealed by selective osmic staining. , 1972, Vision research.

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

[51]  E. Meyer,et al.  Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect , 1996, Cell and Tissue Research.

[52]  J. Milde Graded potentials and action potentials in the large ocellar interneurons of the bee , 1981, Journal of comparative physiology.

[53]  Dr. Willi A. Ribi,et al.  The Neurons of the First Optic Ganglion of the Bee (Apis mellifera) , 1975, Advances in Anatomy, Embryology and Cell Biology / Ergebnisse der Anatomie und Entwicklungsgeschichte / Revues d’anatomie et de morphologie expérimentale.

[54]  Claude Desplan,et al.  The Color-Vision Circuit in the Medulla of Drosophila , 2008, Current Biology.

[55]  D. C. O'Carroll,et al.  Local feedback mediated via amacrine cells in the insect optic lobe , 2004, Journal of Comparative Physiology A.

[56]  W. Ribi The first optic ganglion of the bee , 1985, Cell and Tissue Research.

[57]  N. Strausfeld,et al.  Sign-conserving amacrine neurons in the fly's external plexiform layer , 2005, Visual Neuroscience.