The honeybee Apis mellifera, with a brain of only 960,000 neurons and the ability to perform sophisticated cognitive tasks, has become an excellent model in life sciences and in particular in cognitive neurosciences. It has been used in our laboratories to investigate brain and behavioural asymmetries, i.e., the different functional specializations of the right and the left sides of the brain. It is well known that bees can learn to associate an odour stimulus with a sugar reward, as demonstrated by extension of the proboscis when presented with the trained odour in the so-called Proboscis Extension Reflex (PER) paradigm. Bees recall this association better when trained using their right antenna than they do when using their left antenna. They also retrieve short-term memory of this task better when using the right antenna. On the other hand, when tested for long-term memory recall, bees respond better when using their left antenna. Here we review a series of behavioural studies investigating bees’ lateralization, integrated with electrophysiological measurements to study asymmetries of olfactory sensitivity, and discuss the possible evolutionary origins of these asymmetries. We also present morphological data obtained by scanning electron microscopy and two-photon microscopy. Finally, a behavioural study conducted in a social context is summarised, showing that honeybees control context-appropriate social interactions using their right antenna, rather than the left, thus suggesting that lateral biases in behaviour might be associated with requirements of social life.
References
[1]
Menzel, R.; Giurfa, M. Cognitive architecture of a mini-brain: The honeybee. Trends Cogn. Sci. 2001, 5, 62–71, doi:10.1016/S1364-6613(00)01601-6.
Giurfa, M.; Zhang, S.W.; Jenett, A.; Menzel, R.; Srinivasan, M.V. The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 2001, 410, 930–933, doi:10.1038/35073582.
[4]
Menzel, R. Serial position learning in honeybees. PLoS One 2009, 4, e4694, doi:10.1371/journal.pone.0004694.
[5]
Avarguès-Weber, A.; Giurfa, M. Conceptual learning by miniature brains. Proc. R. Soc. B 2013, 280, 20131907, doi:10.1098/rspb.2013.1907.
[6]
Haase, A.; Rigosi, E.; Frasnelli, E.; Trona, F.; Tessarolo, F.; Vinegoni, C.; Anfora, G.; Vallortigara, G.; Antolini, R. A multimodal approach for tracing lateralization along the olfactory pathway in the honeybee through electrophysiological recordings, morpho-functional imaging, and behavioural studies. EBIOJ 2011, 40, 1247–1258, doi:10.1007/s00249-011-0748-6.
[7]
Rogers, L.J.; Rigosi, E.; Frasnelli, E.; Vallortigara, G. A right antenna for social behaviour in honeybees. Sci. Rep. 2013, 3, 2045.
[8]
Rogers, L.J.; Vallortigara, G.; Andrew, R.J. Divided Brains: The Biology and Behaviour of Brain Asymmetries; Cambridge University Press: Cambridge, UK, 2013.
[9]
Andrew, R.J. The Earliest Origins and Subsequent Evolution of Lateralization. In Comparative Vertebrate Lateralization; Rogers, L.J., Andrew, R.J., Eds.; Cambridge University Press: Cambridge, UK, 2002; pp. 70–93.
MacNeilage, P.F.; Rogers, L.J.; Vallortigara, G. Origins of the left and right brain. Sci. Am. 2009, 301, 60–67, doi:10.1038/scientificamerican0709-60.
[12]
Frasnelli, E.; Vallortigara, G.; Rogers, L.J. Left-right asymmetries of behavioural and nervous system in invertebrates. Neurosci. Biobehav. Rev. 2012, 36, 1273–1291, doi:10.1016/j.neubiorev.2012.02.006.
[13]
Bitterman, M.E.; Menzel, R.; Fietz, A.; Schafer, S. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 1983, 97, 107–119, doi:10.1037/0735-7036.97.2.107.
[14]
Letzkus, P.; Ribi, W.A.; Wood, J.T.; Zhu, H.; Zhang, S.W.; Srinivasan, M.V. Lateralization of olfaction in the honeybee Apis mellifera. Curr. Biol. 2006, 16, 1471–1476, doi:10.1016/j.cub.2006.05.060.
[15]
Letzkus, P.; Boeddeker, N.; Wood, J.T.; Zhang, S.W.; Srinivasan, M.V. Lateralization of visual learning in the honeybee. Biol. Lett. 2008, 4, 16–18, doi:10.1098/rsbl.2007.0466.
[16]
Rogers, L.J.; Vallortigara, G. From antenna to antenna: Lateral shift of olfactory memory in honeybees. PLoS One 2008, 3, e2340, doi:10.1371/journal.pone.0002340.
[17]
Frasnelli, E.; Vallortigara, G.; Rogers, L.J. Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav. Brain Res. 2010, 209, 36–41, doi:10.1016/j.bbr.2010.01.014.
[18]
Rigosi, E.; Frasnelli, E.; Vinegoni, C.; Antolini, R.; Anfora, G.; Vallortigara, G.; Haase, A. Searching for anatomical correlates of olfactory lateralization in the honeybee antennal lobes: A morphological and behavioural study. Behav. Brain Res. 2011, 221, 290–294, doi:10.1016/j.bbr.2011.03.015.
[19]
Frasnelli, E.; Vallortigara, G.; Rogers, L.J. Right-left antennal asymmetry of odour memory recall in three species of Australian stingless bees. Behav. Brain Res. 2011, 224, 121–127, doi:10.1016/j.bbr.2011.05.026.
[20]
Anfora, G.; Frasnelli, E.; Maccagnani, B.; Rogers, L.J.; Vallortigara, G. Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav. Brain Res. 2010, 206, 236–239, doi:10.1016/j.bbr.2009.09.023.
[21]
Anfora, G.; Rigosi, E.; Frasnelli, E.; Ruga, E.; Trona, F.; Vallortigara, G. Lateralization in the invertebrate brain: Left-right asymmetry of olfaction in bumble bee, Bombus terrestris. PLoS One 2011, 6, e18903.
[22]
Kells, A.R.; Goulson, D. Evidence for handedness in bumblebees. J. Insect Behav. 2001, 14, 47–55, doi:10.1023/A:1007897512570.
[23]
Goulson, D.; Park, K.J.; Tinsley, M.C.; Bussière, L.F.; Vallejo-Marin, M. Social learning drives handedness in nectar robbing bumblebees. Behav. Ecol. Sociobiol. 2013, 67, 1141–1150, doi:10.1007/s00265-013-1539-0.
[24]
Hori, S.; Takeuchi, H.; Arikawa, K.; Kinoshita, M.; Ichikawa, N.; Sasaki, M.; Kubo, T. Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J. Comp. Physiol. A 2006, 192, 691–700, doi:10.1007/s00359-005-0091-4.
[25]
Sandoz, J.C.; Menzel, R. Side-specificity of olfactory learning in the honeybee: Generalization between odors and sides. Learn. Memory 2001, 8, 286–294, doi:10.1101/lm.41401.
[26]
Sandoz, J.C.; Hammer, M.; Menzel, R. Side-specificity of olfactory learning in the honeybee: US input side. Learn. Memory 2002, 9, 337–348, doi:10.1101/lm.50502.
Laloi, D.; Pham-Delègue, M.-H. Bumble bees show asymmetrical discrimination between two odors in a classical conditioning procedure. J. Insect Behav. 2004, 17, 385–396, doi:10.1023/B:JOIR.0000031538.15346.e1.
Reinhardt, J.; Sinclair, M.; Srinivasan, M.V.; Claudianos, C. Honeybees Learn Odour Mixtures via a Selection of Key Odorants. PLoS One 2010, 5, e9110, doi:10.1371/journal.pone.0009110.
[31]
Laloi, D.; Bailez, O.; Blight, M.; Roger, B.; Pham-Delègue, M-H.; Wadhams, L.J. Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J. Chem. Ecol. 2000, 26, 2307–2319, doi:10.1023/A:1005522826673.
[32]
Hammer, T.J.; Hata, C.; Nieh, J.C. Thermal learning in the honeybee, Apis mellifera. J. Exp. Biol. 2009, 212, 3928–3934, doi:10.1242/jeb.034140.
[33]
Vallortigara, G.; Rogers, L.J. Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 2005, 28, 575–633.
[34]
Ghirlanda, S.; Vallortigara, G. The evolution of brain lateralization: A game theoretical analysis of population structure. Proc. R. Soc. B 2004, 271, 853–857, doi:10.1098/rspb.2003.2669.
[35]
Ghirlanda, S.; Frasnelli, E.; Vallortigara, G. Intraspecific competition and coordination in the evolution of lateralization. Philos. Trans. R. Soc. Lond. B 2009, 364, 861–866, doi:10.1098/rstb.2008.0227.
[36]
Kawaguchi, L.G.; Ohashi, K.; Toquenaga, Y. Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers. Proc. R. Soc. B 2007, 274, 2661–2667, doi:10.1098/rspb.2007.0860.
[37]
Leadbeater, E.; Chittka, L. Social transmission of nectar-robbing behaviour in bumble-bees. Proc. R. Soc. B 2008, 275, 1669–1674, doi:10.1098/rspb.2008.0270.
[38]
Salerno, G.; Iacovone, A.; Carlin, S.; Frati, F.; Conti, E.; Anfora, G. Identification of sex pheromone components in Trissolcus brochymenae females. J. Insect Physiol. 2012, 58, 1635–1642, doi:10.1016/j.jinsphys.2012.10.003.
[39]
Biswas, S.; Reinhard, J.; Oakeshott, J.; Russell, R.; Srinivasan, M.V.; Claudianos, C. Sensory regulation of neuroligins and neurexin I in the honeybee brain. PLoS One 2010, 5, e9133.
[40]
Frasnelli, E.; Anfora, G.; Trona, F.; Tessarolo, F.; Vallortigara, G. Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav. Brain Res. 2010, 209, 221–225, doi:10.1016/j.bbr.2010.01.046.
[41]
Frasnelli, E.; Rigosi, E.; Anfora, G.; Trona, F.; Vallortigara, G. Left-right asymmetry of olfaction in Apoidea species. In XVI international symposium on olfactory and taste (ISOT), Stockholm, Sweden, 23–27 June 2012.
[42]
Meng, Z.J.; Yan, S.C.; Yang, C.P.; Ruan, C.C. Asymmetrical Distribution of Antennal Sensilla in the Female Anastatus japonicus Ashmead (Hymenoptera: Eupelmidae). Microsc. Res. Techniq. 2012, 75, 1066–1075, doi:10.1002/jemt.22032.
[43]
Sandoz, J.C. Behavioral and neurophysiological study of olfactory perception and learning in honeybees. Neuroscience 2011, 5, 1–20.
[44]
Hourcade, B.; Perisse, E.; Devaud, J.M.; Sandoz, J.C. Long-term memory shapes the primary olfactory center of an insect brain. Learn. Memory 2009, 16, 607–615, doi:10.1101/lm.1445609.
[45]
Zipfel, W.R.; Williams, R.M.; Webb, W.W. Nonlinear magic: Multiphoton microscopy in the biosciences. Nature Biotechnol. 2003, 21, 1369–1377, doi:10.1038/nbt899.
[46]
Winnington, A.P.; Napper, R.M.; Mercer, A.R. Structural Plasticity of Identified glomeruli in the antennal Lobes of Adult Worker Honey Bee. J. Comp. Neurol. 1996, 365, 479–490, doi:10.1002/(SICI)1096-9861(19960212)365:3<479::AID-CNE10>3.0.CO;2-M.
[47]
Galizia, C.G.; N？gler, K.; H？lldobler, B.; Menzel, R. Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Eur. J. Neurosci. 1998, 10, 2964–2974, doi:10.1111/j.1460-9568.1998.00303.x.
[48]
Haase, A.; Rigosi, E.; Trona, F.; Anfora, G.; Vallortigara, G.; Antolini, R.; Vinegoni, C. In-vivo two-photon imaging of the honeybee antennal lobe. Biomed. Opt. Express 2011, 2, 131–138, doi:10.1364/BOE.2.000131.
