Abstract
Honeybees are extensively used to study olfactory learning and memory processes thanks to their ability to discriminate and remember odors and because of their advantages for optophysiological recordings of the circuits involved in memory and odor perception. There are evidences that the encoding of odors in areas of primary sensory processing is not rigid, but undergoes changes caused by olfactory experience. The biological meaning of these changes is focus of intense discussions. Along this review, we present evidences of plasticity related to different forms of learning and discuss its function in the context of olfactory challenges that honeybees have to solve. So far, results in honeybees are consistent with a model in which changes in early olfactory processing contributes to the ability of an animal to recognize the presence of relevant odors and facilitates the discrimination of odors in a way adjusted to its own experience.
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Abbreviations
- AL:
-
Antennal lobe
- ORNs:
-
Olfactory receptor neurons
- LNs:
-
Local neurons
- PNs:
-
Projection neurons
- MBs:
-
Mushroom bodies
- LH:
-
Lateral horn
- lALT:
-
Lateral antennal lobe tract
- mALT:
-
Medial antennal lobe tract
- mlALT:
-
Mediolateral antennal lobe tract
- OA:
-
Octopamine
References
Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437(3):363–383. https://doi.org/10.1002/cne.1289
Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48(3):417–430. https://doi.org/10.1016/j.neuron.2005.10.022
Agarwal M, Guzmán M, Morales-Matos C, Del Valle Díaz RA, Abramson CI, Giray T (2011) Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PLoS ONE 6(9):1–9. https://doi.org/10.1371/journal.pone.0025371
Andrione M, Timberlake BF, Vallortigara G, Antolini R, Haase A (2017) Morphofunctional experience-dependent plasticity in the honeybee brain. Learn Mem 24(12):622–629. https://doi.org/10.1101/lm.046243.117
Arenas A, Giurfa M, Sandoz JC, Hourcade B, Devaud JM, Farina WM (2012) Early olfactory experience induces structural changes in the primary olfactory center of an insect brain. Eur J Neurosci 35(5):682–690. https://doi.org/10.1111/j.1460-9568.2012.07999.x
Bhagavan S, Smith BH (1997) Olfactory conditioning in the honey bee, Apis mellifera: effects of odor intensity. Physiol Behav 61(1):107–117. https://doi.org/10.1016/S0031-9384(96)00357-5
Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45(3):174–183. https://doi.org/10.1002/(SICI)1097-0029(19990501)45:3%3c174::AID-JEMT5%3e3.0.CO;2-U
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol (Washington, D.C. : 1983), 97(2):107–119
Brill MF, Rosenbaum T, Reus I, Kleineidam CJ, Nawrot MP, Rossler W (2013) parallel processing via a dual olfactory pathway in the honeybee. J Neurosci 33(6):2443–2456. https://doi.org/10.1523/jneurosci.4268-12.2013
Brill MF, Meyer A, Rössler W (2015) It takes two-coincidence coding within the dual olfactory pathway of the honeybee. Front Physiol 6:1–14. https://doi.org/10.3389/fphys.2015.00208
Brown SM, Napper RM, Mercer AR (2004) Foraging experience, glomerulus volume, and synapse number: a stereological study of the honey bee antennal lobe. J Neurobiol 60(1):40–50. https://doi.org/10.1002/neu.20002
Campbell RAA, Honegger KS, Qin H, Li W, Demir E, Turner GC (2013) imaging a population code for odor identity in the Drosophila mushroom body. J Neurosci 33(25):10568–10581. https://doi.org/10.1523/JNEUROSCI.0682-12.2013
Chandra SBC, Wright GA, Smith BH (2010) Latent inhibition in the honey bee, Apis mellifera: is it a unitary phenomenon? Anim Cogn 13(6):805–815. https://doi.org/10.1007/s10071-010-0329-6
Chen J-Y, Marachlian E, Assisi C, Huerta R, Smith BH, Locatelli F, Bazhenov M (2015) Learning modifies odor mixture processing to improve detection of relevant components. J Neurosci 35(1):179–197. https://doi.org/10.1523/JNEUROSCI.2345-14.2015
Claudianos C, Lim J, Young M, Yan S, Cristino AS, Newcomb RD, Reinhard J (2014) Odor memories regulate olfactory receptor expression in the sensory periphery. Eur J Neurosci 39(10):1642–1654. https://doi.org/10.1111/ejn.12539
Conchou L, Lucas P, Meslin C, Proffit M, Staudt M, Renou M. (2019) Insect odorscapes: From plant volatiles to natural olfactory scenes. Front Physiol 10(JUL). https://doi.org/10.3389/fphys.2019.00972
Das S, Sadanandappa MK, Dervan A, Larkin A, Lee JA, Sudhakaran IP, Ramaswamia M (2011) Plasticity of local GABAergic interneurons drives olfactory habituation. Proc Natl Acad Sci USA 108(36):2–10. https://doi.org/10.1073/pnas.1106411108
de Jong R, Pham-Delègue MH (1991) Electroantennogram responses related to olfactory conditioning in the honey bee (Apis mellifera ligustica). J Insect Physiol 37(4):319–324. https://doi.org/10.1016/0022-1910(91)90066-9
Deisig N, Giurfa M, Lachnit H, Sandoz JC (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24(4):1161–1174. https://doi.org/10.1111/j.1460-9568.2006.04959.x
Deisig N, Giurfa M, Sandoz JC (2010) Antennal lobe processing increases separability of odor mixture representations in the honeybee. J Neurophysiol 103(4):2185–2194. https://doi.org/10.1152/jn.00342.2009
Denker M, Finke R, Schaupp F, Grün S, Menzel R (2010) Neural correlates of odor learning in the honeybee antennal lobe. Eur J Neurosci 31(1):119–133. https://doi.org/10.1111/j.1460-9568.2009.07046.x
El Hassani AK, Giurfa M, Gauthier M, Armengaud C (2008) Inhibitory neurotransmission and olfactory memory in honeybees. Neurobiol Learn Mem 90(4):589–595. https://doi.org/10.1016/j.nlm.2008.07.018
Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the bee. Apis mellifera Physiol Entomol 5(4):343–358. https://doi.org/10.1111/j.1365-3032.1980.tb00244.x
Esslen J, Kaissling K (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene ( Apis mellifera L .), 251, 227–228
Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2(1):74–78. https://doi.org/10.1038/4576
Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23(12):5370–5380. https://doi.org/10.1523/jneurosci.23-12-05370.2003
Fernandez PC, Locatelli FF, Person-Rennell N, Deleo G, Smith BH (2009) Associative conditioning tunes transient dynamics of early olfactory processing. J Neurosci Off J Soc Neurosci 29(33):10191–10202. https://doi.org/10.1523/JNEUROSCI.1874-09.2009
Flanagan D, Mercer AR (1989a) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera : Apidae). Int J Insect Morphol Embryol 18(2–3):145–159. https://doi.org/10.1016/0020-7322(89)90023-8
Flanagan D, Mercer AR (1989b) Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164(4):483–494. https://doi.org/10.1007/BF00610442
Free JB (1987) Pheromones of Social Bees. Chapman and Hall, London
Friedrich A, Thomas U, Müller U (2004) Learning at different satiation levels reveals parallel functions for the cAMP-protein kinase A cascade in formation of long-term memory. J Neurosci 24(18):4460–4468. https://doi.org/10.1523/JNEUROSCI.0669-04.2004
Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295(3):383–394. https://doi.org/10.1007/s004410051245
Galizia CG, Sachse S, Rappert A, Menzel R (1999) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2(5):473–478. https://doi.org/10.1038/8144
Galizia CG, Kimmerle B (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190(1):21–38. https://doi.org/10.1007/s00359-003-0469-0
Galizia C, Vetter R (2004) Optical methods for analyzing odor-evoked activity in the insect brain. https://doi.org/10.1201/9781420039429.ch13
Galizia CG, Rössler W (2009) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55(1):399–420. https://doi.org/10.1146/annurev-ento-112408-085442
Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55(1):399–420. https://doi.org/10.1146/annurev-ento-112408-085442
Getz WM, Akers RP (1993) Olfactory response characteristics and tuning structure of placodes in the honey bee Apis mellifera L. Apidologie 24(3):195–217. https://doi.org/10.1051/apido:19930303
Girardin CC, Kreissl S, Galizia CG (2012) Inhibitory connections in the honeybee antennal lobe are spatially patchy. J Neurophysiol (October 2012), 332–343. https://doi.org/10.1152/jn.01085.2011
Grohmann L, Blenau W, Erber J, Ebert PR, Strünker T, Baumann A (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J Neurochem 86(3):725–735. https://doi.org/10.1046/j.1471-4159.2003.01876.x
Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435(4):474–489. https://doi.org/10.1002/cne.1045
Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3(4):0718–0732. https://doi.org/10.1371/journal.pbio.0030060
Haenicke J, Yamagata N, Zwaka H, Nawrot M, Menzel R (2018) Neural correlates of odor learning in the presynaptic microglomerular circuitry in the honeybee mushroom body Calyx. ENeuro 5(3):1–13. https://doi.org/10.1523/ENEURO.0128-18.2018
Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366(6450):59–63. https://doi.org/10.1038/366059a0
Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees, 146–156. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC311245/pdf/x2.pdf
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20(1):595–631. https://doi.org/10.1146/annurev.neuro.20.1.595
Honegger KS, Campbell RAA, Turner GC (2011) Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body. J Neurosci 31(33):11772–11785. https://doi.org/10.1523/JNEUROSCI.1099-11.2011
Hourcade B, Perisse E, Devaud JM, Sandoz JC (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learn Mem 16(10):607–615. https://doi.org/10.1101/lm.1445609
Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, Vosshall LB (2014) A systematic nomenclature for the insect brain. Neuron 81(4):755–765. https://doi.org/10.1016/j.neuron.2013.12.017
Jernigan CM, Halby R, Gerkin RC, Sinakevitch I, Locatelli F, Smith BH (2020) Experience-dependent tuning of early olfactory processing in the adult honey bee, Apis mellifera. J Exp Biol 223(1). https://doi.org/10.1242/jeb.206748
Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285. Retrieved from https://doi.org/10.1038/387285a0
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(6):933–952. https://doi.org/10.1002/cne.21158
Klappenbach M, Kaczer L, Locatelli F (2013) Neurobiology of Learning and Memory Dopamine interferes with appetitive long-term memory formation in honey bees. Neurobiol Learn Mem 106:230–237. Retrieved from https://doi.org/10.1016/j.nlm.2013.09.011
Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348(4):583–595. https://doi.org/10.1002/cne.903480408
Krofczik S, Menzel R, Nawrot MP (2009) Rapid odor processing in the honeybee antennal lobe network. Front Comput Neurosci, 2(JAN), 1–13. https://doi.org/10.3389/neuro.10.009.2008
Linster C, Sachse S, Galizia CG (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 93(6):3410–3417. https://doi.org/10.1152/jn.01285.2004
Locatelli FF, Fernandez PC, Villareal F, Muezzinoglu K, Huerta R, Galizia CG, Smith BH (2013) Nonassociative plasticity alters competitive interactions among mixture components in early olfactory processing. Eur J Neurosci 37(1):63–79. https://doi.org/10.1111/ejn.12021
Locatelli FF, Fernandez PC, Smith BH (2016) Learning about natural variation of odor mixtures enhances categorization in early olfactory processing. J Exp Biol 219(17):2752–2762. https://doi.org/10.1242/jeb.141465
Menzel R (1999) Memory dynamics in the honeybee. Journal of Comparative Physiology - A Sensory, Neural, and Behavioral Physiology 185(4):323–340. https://doi.org/10.1007/s003590050392
Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13(11):758–768. https://doi.org/10.1038/nrn3357
Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 188(5):359–370. https://doi.org/10.1007/s00359-002-0310-1
Müller U (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27(1):159–168. https://doi.org/10.1016/S0896-6273(00)00017-9
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(43):11736–11747. https://doi.org/10.1523/JNEUROSCI.2216-07.2007
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. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 192(10):1083–1103. https://doi.org/10.1007/s00359-006-0152-3
Ramírez G, Fagundez C, Grosso JP, Argibay P, Arenas A, Farina WM (2016) Odor experiences during preimaginal stages cause behavioral and neural plasticity in adult honeybees. Front Behav Neurosci 10(JUN), 1–14. https://doi.org/10.3389/fnbeh.2016.00105
Rath L, Giovanni Galizia C, Szyszka P (2011) Multiple memory traces after associative learning in the honey bee antennal lobe. Eur J Neurosci 34(2):352–360. https://doi.org/10.1111/j.1460-9568.2011.07753.x
Rein J, Mustard JA, Strauch M, Smith BH, Galizia CG (2013) Octopamine modulates activity of neural networks in the honey bee antennal lobe. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199(11):947–962. https://doi.org/10.1007/s00359-013-0805-y
Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee Apis mellifera : Expansion of the odorant, but not gustatory, receptor family 1395–1403 https://doi.org/10.1101/gr.5057506
Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87(2):1106–1117. https://doi.org/10.1152/jn.00325.2001
Sachse S, Galizia CG (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18(8):2119–2132. https://doi.org/10.1046/j.1460-9568.2003.02931.x
Sachse S, Peele P, Silbering AF, Gühmann M, Galizia CG (2006) Role of histamine as a putative inhibitory transmitter in the honeybee antennal lobe. Front Zool 3:1–7. https://doi.org/10.1186/1742-9994-3-22
Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Vosshall LBB (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56(5):838–850. https://doi.org/10.1016/j.neuron.2007.10.035
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(4):1137–1148. https://doi.org/10.1016/S0306-4522(03)00384-1
Sandoz JC (2011) Behavioral and neurophysiological study of olfactory perception and learning in honeybees. Front Syst Neurosci 5(DECEMBER 2011), 1–20. https://doi.org/10.3389/fnsys.2011.00098
Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23(33):10495–10502. https://doi.org/10.1523/jneurosci.23-33-10495.2003
Sigg D, Thompson CM, Mercer AR (1997) Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). J Neurosci 17(18):7148–7156. https://doi.org/10.1523/jneurosci.17-18-07148.1997
Sinakevitch IT, Smith AN, Locatelli F, Huerta R, Bazhenov M, Smith BH (2013) Apis mellifera octopamine receptor 1 (AmOA1) expression in antennal lobe networks of the honey bee (Apis mellifera) and fruit fly (Drosophila melanogaster). Front Syst Neurosci 7(October):1–19. https://doi.org/10.3389/fnsys.2013.00070
Sinakevitch I, Bjorklund GR, Newbern JM, Gerkin RC, Smith BH (2018) Comparative study of chemical neuroanatomy of the olfactory neuropil in mouse, honey bee, and human. Biol Cybern 112(1–2):127–140. https://doi.org/10.1007/s00422-017-0728-8
Smith BH, Huerta R, Bazhenov M, Sinakevitch I (2012) Distributed Plasticity for Olfactory Learning and Memory in the Honey Bee Brain. In Galizia CG, Eisenhardt D, Giurfa M (Eds) Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel (pp. 393–408). Dordrecht: Springer Netherlands. https://doi.org/10.1007/978-94-007-2099-2_30
Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odor discrimination on desynchronization of odor–encoding neural assemblies. Nature 390(August):70–74
Strauch M, Ditzen M, Galizia CG (2012) Kee** their distance? Odor response patterns along the concentration range. Front Syst Neurosci 6(October):1–13. https://doi.org/10.3389/fnsys.2012.00071
Strube-Bloss MF, Nawrot MP, Menzel R (2011) Mushroom body output neurons encode odor-reward associations. J Neurosci 31(8):3129–3140. https://doi.org/10.1523/JNEUROSCI.2583-10.2011
Strube-Bloss MF, Herrera-Valdez MA, Smith BH (2012) Ensemble response in mushroom body output neurons of the honey bee outpaces spatiotemporal odor processing two synapses earlier in the antennal lobe. PLoS ONE 7(11):1–13. https://doi.org/10.1371/journal.pone.0050322
Szyszka P (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94(5):3303–3313. https://doi.org/10.1152/jn.00397.2005
Takeda K (1961).Classical conditioned response in the honey bee. J Insect Physiol 6(3), 168–179. https://doi.org/10.1016/0022-1910(61)90060-9
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(3). https://doi.org/10.1371/journal.pone.0000288
Winnington AP, Napper RM, Mercer AR (1996) Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J Comp Neurol 365(3):479–490. https://doi.org/10.1002/(SICI)1096-9861(19960212)365:3%3c479::AID-CNE10%3e3.0.CO;2-M
Wright GA, Lutmerding A, Dudareva N, Smith BH (2005) Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191(2):105–114. https://doi.org/10.1007/s00359-004-0576-6
Wright GA, Skinner BD, Smith BH (2002) Ability of honeybee, Apis mellifera, to detect and discriminate odors of varieties of canola (Brassica rapa and Brassica napus) and snapdragon flowers (Antirrhinum majus). J Chem Ecol 28(4):721–740. https://doi.org/10.1023/A:1015232608858
Wright GA, Mustard JA, Simcock NK, Ross-Taylor AAR, McNicholas LD, Popescu A, Marion-Poll F (2010) Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr Biol 20(24):2234–2240. https://doi.org/10.1016/j.cub.2010.11.040
Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning: Memory trace formation by synaptic recruitment. Neuron 42(3):437–449. https://doi.org/10.1016/S0896-6273(04)00217-X
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Authors thank two anonymous reviewers for insightful comments and suggestions.
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The authors have been supported by grants from ANPCyT: Agencia Nacional de Promoción Cientifica y Tecnica, Argentina: PICT 2016-1755 to EM. ANPCyT PICT 2017-1285, CONICET and University of Buenos Aires to MK. ANPCyT PICT 2017-2284, CONICET and University of Buenos Aires to FL.
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Marachlian, E., Klappenbach, M. & Locatelli, F. Learning-dependent plasticity in the antennal lobe improves discrimination and recognition of odors in the honeybee. Cell Tissue Res 383, 165–175 (2021). https://doi.org/10.1007/s00441-020-03396-2
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DOI: https://doi.org/10.1007/s00441-020-03396-2