Abstract
Recent studies have revealed asymmetries between the left and right sides of the brain in invertebrate species. Here we present a review of a series of recent studies from our laboratories, aimed at tracing asymmetries at different stages along the honeybee’s (Apis mellifera) olfactory pathway. These include estimates of the number of sensilla present on the two antennae, obtained by scanning electron microscopy, as well as electroantennography recordings of the left and right antennal responses to odorants. We describe investigative studies of the antennal lobes, where multi-photon microscopy was used to search for possible morphological asymmetries between the two brain sides. Moreover, we report on recently published results obtained by two-photon calcium imaging for functional mapping of the antennal lobe aimed at comparing patterns of activity evoked by different odours. Finally, possible links to the results of behavioural tests, measuring asymmetries in single-sided olfactory memory recall, are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ades C, Ramires EN (2002) Asymmetry of leg use during prey handling in the spider Scytodes globula (Scytodidae). J Insect Behav 15:563–570. doi:10.1023/A:1016337418472
Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G (2010) Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav Brain Res 206:236–239. doi:10.1016/j.bbr.2009.09.023
Biswas S, Reinhard J, Oakeshott J, Russell R, Srinivasan MV et al (2010) Sensory regulation of neuroligins and neurexin i in the honeybee brain. PLoS ONE 5(2):e9133. doi:10.1371/journal.pone.0009133
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119. doi:10.1037/0735-7036.97.2.107
Boch R, Shearer DA, Stone BC (1962) Identification of isoamyl acetate as an active component in the sting pheromone of the honey bee. Nature 195:1018–1020. doi:10.1038/1951018b0
Boeckh J (1974) Die Reaktion olfaktorischer Neurone im Deutocerebrum von Insekten im Vergleich zu den Antwortmustern der Geruchssinneszellen. J Comp Physiol A 90:183–205. doi:10.1007/BF00694484
Broca P (1861) Perte de la parole, ramollissement chronique et destruction partielle du lobe antérieur gauche du cerveau. Bull Soc Anthropol 2:235–238
Bucher D, Scholz M, Stetter M, Obermayer K, Pfluger HJ (2000) Correction methods for three-dimensional reconstructions from confocal images: I. tissue shrinking and axial scaling. J Neurosci Methods 100:135–143. doi:10.1016/S0165-0270(00)00245-4
Denk W, Svoboda K (1997) Photon upmanship: why multiphoton imaging is more than a gimmick. Neuron 18:351–357. doi:10.1016/S0896-6273(00)81237-4
Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73–76. doi:10.1126/science.2321027
Dietz A, Humphreys J (1971) Scanning electron microscopic studies of antennal receptors of the worker honey bee, including Sensilla campaniformia. Ann Entomol Soc Amer 64:919–925
Duistermars BJ, Chow DM, Frye Ma (2009) Flies require bilateral sensory input to track odor gradients in flight. Curr Biol 19(15):1301–1307. doi:10.1016/j.cub.2009.06.022
Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representation of odours in the insect brain. Nat Neurosci 2:74–78. doi:10.1038/4576
Fernandez PC, Locatelli FF, Person-Rennell N, Deleo G, Smith BH (2009) Associative Conditioning tunes transient dynamics of early olfactory processing. J Neurosci 29:10191–10202. doi:10.1523/JNEUROSCI.1874-09.2009
Franke T (2009) In vivo 2-photon calcium imaging of olfactory interneurons in the honeybee antennal lobe. PhD thesis, Freien Universität Berlin
Frasnelli E, Anfora G, Trona F, Tessarolo F, Vallortigara G (2010a) Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav Brain Res 209:221–225. doi:10.1016/j.bbr.2010.01.046
Frasnelli E, Vallortigara G, Rogers LJ (2010b) Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav Brain Res 209:36–41. doi:10.1016/j.bbr.2010.01.014
Galizia CG, Szyszka P (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol Exp Appl 128(1):81–92. doi:10.1111/j.1570-7458.2007.00661.x
Galizia CG, Vetter R (2004) Optical methods for analyzing odor-evoked activity in the insect brain. In: Christensen TA (ed) Advances in Insect Sensory Neuroscience. CRC press, Boca Raton, pp 349–392. doi:10.1201/9781420039429.ch13
Galizia CG, Nägler K, Hölldobler B, Menzel R (1998) Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Europ J Neurosci 10:2964–2974. doi:10.1111/j.1460-9568.1998.00303.x
Galizia CG, Sachse S, Rappert A, Menzel R (1999a) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473–478. doi:10.1038/8144
Galizia CG, McIlwrath SL, Menzel R (1999b) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295: 383–394. http://neuro.uni-konstanz.de/23beemorph/default.html
Gelperin A, Flores J (1997) Vital staining from dye-coated microprobes identifies new olfactory interneurons for optical and electrical recording. J Neurosci Methods 72:97–108. doi:10.1016/S0165-0270(96)02169-3
Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824. doi:10.1007/s00359-007-0235-9
Grynkiewicz G, Poenie M, Tsien RY (1985) A New Generation of Ca2+ Indicators with Greatly Improved Fluorescence Properties. J Biol Chem 260:3440–3450
Haase A, Rigosi E, Trona F, Anfora G, Vallortigara G, Antolini R, Vinegoni C (2011) In vivo two-photon imaging of the honey bee antennal lobe. Biomed Opt Express 2:131–138. doi:10.1364/BOE.2.000131
Hobert O, Johnston RJ Jr, Chang S (2002) Left–right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat Rev Neurosci 3:629–640. doi:10.1038/nrn897
Hourcade B, Perisse E, Devaud JM, Sandoz JC (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learn Mem 16:607–615. doi:10.1101/lm.1445609
Junek S, Kludt E, Wolf F, Schild D (2010) Olfactory Coding with Patterns of Response Latencies. Neuron 67:872–884. doi:10.1016/j.neuron.2010.08.005
Kaissling KE, Thorson J (1980) Insect olfactory sensilla: structural, chemical and electrical aspects of the functional organization. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for Neurotransmitters. Hormones, and Pheromones in Insects, Elsevier/North-Holland Biomedical Press, pp 261–282
Kelber C, Rössler W, Kleineidam CJ (2006) Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395–405. doi:10.1002/cne.20930
Kells AR, Goulson D (2001) Evidence for handedness in bumblebees. J Insect Behav 14:47–55. doi:10.1023/A:1007897512570
Krofczik S, Menzel R, and Nawrot MP (2009) Rapid odor processing in the honeybee antennal lobe network. Front Comput Neurosci. doi:10.3389/neuro.10.009.2008
Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Zool 13:458–464
Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895. doi:10.1038/nrn964
Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV (2006) Lateralization of Olfaction in the Honeybee Apis mellifera. Curr Biol 16:1471–1476. doi:10.1016/j.cub.2006.05.060
Lieke EE (1993) Optical recording of neuronal activity in the insect central nervous system: odorant coding by the antennal lobes of honeybees Eur J Neurosci 5:49–55. doi:10.1111/j.1460-9568.1993.tb00204.x
MacNeilage PF, Rogers LJ, Vallortigara G (2009) Origins of the left and right brain. Sci Am 301:60–67. doi:10.1038/scientificamerican0709-60
Matsumoto SG, Hildebrand JG (1981) Olfactory Mechanisms in the Moth Manduca sexta: Response Characteristics and Morphology of Central Neurons in the Antennal Lobes. Proc R Soc Lond B 213:249–277
Menzel R, Giurfa M (2001) Cognitive architecture of a mini-brain: the honeybee. Trends Cogn Sci 5:62–71. doi:10.1016/S1364-6613(00)01601-6
Menzel R, Müller U (1996) Learning and memory in honeybees: From behavior to neural substrates. Ann Rev Neurosci 19:379–404. doi:10.1146/annurev.ne.19.030196.002115
Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188:359–370. doi:10.1007/s00359-002-0310-1
Nottebohm F (1970) Ontogeny of bird song. Science 167:950–956. doi:10.1126/science.167.3920.950
Pavlov IP (1927) Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex. Oxford University Press, London
Peele P, Ditzen M, Menzel R, Galizia CG (2006) Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J Comp Physiol A 192:1083–1103. doi:10.1007/s00359-006-0152-3
Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE 5:e9110. doi:10.1371/journal.pone.0009110
Rigosi E, Frasnelli E, Vinegoni C, Antolini R, Anfora G, Vallortigara G, Haase A (2011) Searching for anatomical correlates of olfactory lateralization in the honeybee antennal lobes: a morphological and behavioural study. Behav Brain Res 221:290–294. doi:10.1016/j.bbr.2011.03.015
Rogers LJ, Anson JM (1979) Lateralisation of function in the chicken forebrain. Pharmacol Biochem Be 10:679–686. doi:10.1016/0091-3057(79)90320-4
Rogers LJ, Vallortigara G (2008) From antenna to antenna: lateral shift of olfactory memory recall by honeybees. PLoS ONE 3(6):e2340. doi:10.1371/journal.pone.0002340
Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc Biol Sci 271(Suppl 6):S420–S422. doi:10.1098/rsbl.2004.0200
Roussel E, Sandoz JC, Giurfa M (2010) Searching for learning-dependent changes in the antennal lobe: simultaneous recording of neural activity and aversive olfactory learning in honeybees. Front Behav Neurosci 4:155. doi:10.3389/fnbeh.2010.00155
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. doi:10.1046/j.1460-9568.1999.00826.x
Sandoz JC, Menzel R (2001) Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. Learn Mem 8:286–294. doi:10.1101/lm.41401
Sandoz JC, Galizia CG, Menzel R (2003) Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes. Neuroscience 120:1137–1148. doi:10.1016/S0306-4522(03)00384-1
Schneider D (1957) Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. J Comp Physiol A. doi:10.1007/BF00298148
Sigg D, Thompson CM, Mercer AR (1997) Activity-dependent changes to the brain and behaviour of the honey bee. Apis mellifera (L.). J Neurosci 17:7148–7156
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633. doi:10.1017/S0140525X05000105
Whitehead AT, Larsen JR (1976) Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera : Apidae). Int J Insect Morphol Embryol 5:301–315. doi:10.1016/0020-7322(76)90030-1
Winnington AP, Napper RM, Mercer AR (1996) Structural plasticity of identified glomeruli in the antennal lobes of adult worker honey bee. J Comp Neurol 365:479–490. doi:10.1002/(SICI)1096-9861(19960212)365:3<479:AID-CNE10>3.0.CO;2-M
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. doi:10.3389/neuro.06.016.2009
Acknowledgments
This work has been realised also thanks to the support from the Provincia Autonoma di Trento and the Fondazione Cassa di Risparmio di Trento e Rovereto. C.V. acknowledges Provincia Autonoma di Trento (project COMFI) and National Institutes of Health grant RO1EB006432.
Author information
Authors and Affiliations
Corresponding author
Additional information
Special Issue: SIBPA 2011 Meeting.
Rights and permissions
About this article
Cite this article
Haase, A., Rigosi, E., Frasnelli, E. et al. A multimodal approach for tracing lateralisation along the olfactory pathway in the honeybee through electrophysiological recordings, morpho-functional imaging, and behavioural studies. Eur Biophys J 40, 1247–1258 (2011). https://doi.org/10.1007/s00249-011-0748-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-011-0748-6