Abstract
For more than a century, honey bees have constituted a major model for the study of olfactory detection, processing, learning and memory. This chapter reviews major advances based on three main approaches. Firstly, we address the experimental study of bees’ olfactory behavior, from early experiments on free-flying workers until laboratory-based training protocols on restrained individuals. We describe bees’ impressive discrimination and generalization abilities depending on odor quality and quantity, their capacity to grant special properties to olfactory mixtures as well as to recognize individual components. Secondly, we provide a detailed description of the olfactory pathways of the bee brain that subtend these behaviors, based on anatomical and immunochemical studies. We show how odors are detected by olfactory receptors carried by receptor neurons in the antenna, which convey information to a first processing relay, the antennal lobe (AL). We describe processing circuits within this structure and show how olfactory information is then conducted to higher-order centres, the mushroom bodies (MBs) and the lateral horn (LH), following different pathways through the brain. We finish by discussing the structure of the MBs, their local circuits and output connections and how they may be linked to motor output. Thirdly, we show how functional approaches based on the recording of odor-evoked activity in the bee brain allow following the series of transformations of the olfactory representation through its different centers. Data from electrophysiological and optical imaging approaches are reviewed. Doing so, we explain how coupling behavior with functional approaches allows understanding the perceptual representation of odors.
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Abbreviations
- CS:
-
Conditioned stimulus
- GABA:
-
Gamma-aminobutyric acid
- PER:
-
Proboscis extension reflex
- US:
-
Unconditioned stimulus
References
Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437:363–383
Akers RP, Getz WM (1992) A test of identified response classes among olfactory receptor neurons in the honey-bee worker. Chem Senses 17:191–209
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees. J Comp Psychol 97:107–119
Deisig N, Lachnit H, Sandoz JC, Lober K, Giurfa M (2003) A modified version of the unique cue theory accounts for olfactory compound processing in honeybees. Learn Mem 10:199–208
Deisig N, Giurfa M, Lachnit H, Sandoz JC (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24:1161–1174
Deisig N, Giurfa M, Sandoz JC (2010) Antennal lobe processing increases separability of odor mixture representations in the honeybee. J Neurophysiol 103:2185–2194
Ditzen M, Evers JF, Galizia CG (2003) Odor similarity does not influence the time needed for odor processing. Chem Senses 28:781–789
Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphology 83:227–251
Flanagan D, Mercer AR (1989) Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164:483–494
Fonta C, Sun XJ, Masson C (1993) Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18(2):101–119
Galizia CG (2008) Insect olfaction. In: Smith DV, Firestein S, Beauchamp GK (eds) The senses, a comprehensive reference. Elsevier, London, pp 725–769
Galizia CG, Kimmerle B (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol A 190:21–38
Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired using confocal microscopy. Cell Tissue Res 295:383–394
Getz WM, Smith KB (1991) Olfactory perception in honeybees: concatenated and mixed odorant stimuli, concentration, and exposure effects. J Comp Physiol A 169:215–230
Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:e60
Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63
Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203
Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288
Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933–952
Kramer E (1976) The orientation of walking honeybees in odour fields with small concentration gradients. Physiol Entomol 1:27–37
Krofczik S, Menzel R, Nawrot MP (2009) Rapid odor processing in the honeybee antennal lobe network. Front Comput Neurosci 2:9
Lacher V, Schneider D (1963) Elektrophysiologischer Nachweis der Riechfunktion von Porenplatten (Sensilla placodea) auf den Antennen der Drohne und der Arbeitsbiene (Apis mellifera L.). Z vergl Physiol 47:274–278
Laska M, Galizia CG, Giurfa M, Menzel R (1999) Olfactory discrimination ability and odor structure-activity relationships in honeybees. Chem Senses 24:429–438
Mauelshagen J (1993) Neural correlates of olfactory learning paradigms in an identified Âneuron in the honeybee brain. J Neurophysiol 69:609–625
Menzel R, Greggers U, Hammer M (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Lewis AC (ed) Insect learning. Chapman & Hall, New York/London, pp 79–125
Mobbs PG (1982) The brain of the honeybee Apis mellifera I.The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298:309–354
Müller D, Abel R, Brandt R, Zockler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188:359–370
Okada R, Rybak J, Manz G, Menzel R (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J Neurosci 27:11736–11747
Pelz C, Gerber B, Menzel R (1997) Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J Exp Biol 200:837–847
Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359–365
Pham-Delègue MH, Etiévant P, Guichard E, Masson C (1989) Sunflower volatiles involved in honeybee discrimination among genotypes and flowering stages. J Chem Ecol 15:329–343
Pham-Delègue MH, Bailez O, Blight MM, Masson C, Picard-Nizou AL, Wadhams LJ (1993) Behavioral discrimination of oilseed rape volatiles by the honeybee Apis mellifera L. Chem Senses 18:483–494
Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS One 5:e9110
Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403
Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334:444–465
Sachse S, Galizia CG (2002) The Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117
Sachse S, Galizia CG (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119–2132
Sachse S, Rappert A, Galizia CG (1999) The Spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11:3970–3982
Sandoz JC, Pham-Delegue MH, Renou M, Wadhams LJ (2001) Asymmetrical generalisation between pheromonal and floral odours in appetitive olfactory conditioning of the honey bee (Apis mellifera L.). J Comp Physiol A 187:559–568
Smith BH (1998) Analysis of interaction in binary odorant mixtures. Physiol Behav 65:397–407
Smith BH, Menzel R (1989) The use of electromyogram recordings to quantify odourant discrimination in the honey bee, Apis mellifera. J Insect Physiol 35:369–375
Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74
Strausfeld NJ (2002) Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4–33
Szyszka P, Ditzen M, Galkin A, Galizia CG, Menzel R (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94:3303–3313
Vareschi E (1971) Duftunterscheidung bei der Honigbiene - Einzelzell-Ableitungen und Verhaltensreaktionen. Z vergl Physiol 75:143–173
Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2:e288
von Frisch K (1919) Über den Geruchsinn der Biene und seine blütenbiologische Bedeutung. Zoologisches Jahrbuch Teil Physiologie 37:1–238
Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102(2):147–159
Wadhams LJ, Blight MM, Kerguelen V, Métayer ML, Marion-Poll F, Masson C, Pham-Delègue MH, Woodcock CM (1994) Discrimination of oilseed rape volatiles by honey bee: novel combined gas chromatographic-electrophysiological behavioral assay. J Chem Ecol 20:3221–3231
Wright GA, Smith BH (2004) Different thresholds for detection and discrimination of odors in the honey bee (Apis mellifera). Chem Senses 29:127–135
Yamagata N, Schmuker M, Szyszka P, Mizunami M, Menzel R (2009) Differential odor processing in two olfactory pathways in the honeybee. Front Syst Neurosci 3:16
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Sandoz, JC. (2012). Olfaction in Honey Bees: From Molecules to Behavior. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_19
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