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Brief sensory experience differentially affects the volume of olfactory brain centres in a moth

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Abstract

Experience modifies behaviour in animals so that they adapt to their environment. In male noctuid moths, Spodoptera littoralis, brief pre-exposure to various behaviourally relevant sensory signals modifies subsequent behaviour towards the same or different sensory modalities. Correlated with a behavioural increase in responses of male moths to the female-emitted sex pheromone after pre-exposure to olfactory, acoustic or gustatory stimuli, an increase in sensitivity of olfactory neurons within the primary olfactory centre, the antennal lobe, is found for olfactory and acoustic stimuli, but not for gustatory stimuli. Here, we investigated whether anatomical changes occurring in the antennal lobes and in the mushroom bodies (the secondary olfactory centres) possibly correlated with the changes observed in behaviour and in olfactory neuron physiology. Our results showed that significant volume changes occurred in glomeruli (olfactory units) responsive to sex pheromone following exposure to both pheromone and predator sounds. The volume of the mushroom body input region (calyx) also increased significantly after pheromone and predator sound treatment. However, we found no changes in the volume of antennal lobe glomeruli or of the mushroom body calyx after pre-exposure to sucrose. These findings show a relationship of antennal lobe sensitivity changes to the pheromone with changes in the volume of the related glomeruli and the output area of antennal lobe projection neurons elicited by sensory cues causing a behavioural change. Behavioural changes observed after sucrose pre-exposure must originate from changes in higher integration centres in the brain.

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References

  • Anderson P, Sadek M, Hansson B (2003) Pre-exposure modulates attraction to sex pheromone in a moth. Chem Senses 28:285–291

    Article  CAS  PubMed  Google Scholar 

  • Anderson P, Hansson BS, Nilsson U, Han Q, Sjöholm M, Skals N, Anton S (2007) Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth. Chem Senses 32:483–491

    Article  CAS  PubMed  Google Scholar 

  • Anton S, Evengaard K, Barrozo RB, Anderson P, Skals N (2011) Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect. Proc Natl Acad Sci U S A 108:3401–3405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown S, Napper R, Mercer A (2004) Foraging experience, glomerulus volume, and synapse number: a stereological study of the honey bee antennal lobe. J Neurobiol 60:40–50

    Article  PubMed  Google Scholar 

  • Busto GUG, Cervantes-Sandoval II, Davis RLR (2010) Olfactory learning in Drosophila. Annu Rev Physiol 25:338–346

    CAS  Google Scholar 

  • Couton L, Minoli S, Kieu K, Anton S, Rospars J-P (2009) Constancy and variability of identified glomeruli in antennal lobes: computational approach in Spodoptera littoralis. Cell Tissue Res 337:491–511

    Article  PubMed  Google Scholar 

  • Devaud J-M, Acebes A, Ferrús A (2001) Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila. J Neurosci 21:6274–6282

    CAS  PubMed  Google Scholar 

  • Devaud J-M, Acebes A, Ramaswami M, Ferrús A (2003) Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J Neurobiol 56:13–23

    Article  PubMed  Google Scholar 

  • Fan R, Anderson P, Hansson B (1997) Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera : Noctuidae). J Exp Biol 200:2969–2976

    PubMed  Google Scholar 

  • Farris SM, Robinson GE, Fahrbach SE (2001) Experience- and age-related ourgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395–6404

    CAS  PubMed  Google Scholar 

  • Fox K, Wong R (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48:465–477

    Article  CAS  PubMed  Google Scholar 

  • Giurfa MM (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824

    Article  Google Scholar 

  • Groh C, Meinertzhagen IA (2010) Brain plasticity in Diptera and Hymenoptera. Frontiers Biosci 2:268–288

    Google Scholar 

  • Groh C, Lu Z, Meinertzhagen IA, Rössler W (2012) Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera. J Comp Neurol 520:3509–3527

    Article  PubMed  Google Scholar 

  • Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435:474–489

    Article  CAS  PubMed  Google Scholar 

  • Grubb MS, Thompson ID (2004) The influence of early experience on the development of sensory systems. Curr Opin Neurobiol 14:503–512

    Article  CAS  PubMed  Google Scholar 

  • Guerrieri F, Gemeno C, Monsempes C, Anton S, Jacquin-Joly E, Lucas P, Devaud J-M (2012) Experience-dependent modulation of antennal sensitivity and input to antennal lobes in male moths (Spodoptera littoralis) pre-exposed to sex pheromone. J Exp Biol 215:2334–2341

    Article  CAS  PubMed  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    Article  CAS  PubMed  Google Scholar 

  • Han Q, Hansson BS, Anton S (2005) Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth, Spodoptera littoralis. J Comp Physiol A 191:521–528

    Article  CAS  Google Scholar 

  • Hartlieb E, Hansson B, Anderson P (1999) Sex or food? Appetetive learning of sex odors in a male moth. Naturwissenschaften 86:396–399

    Article  CAS  Google Scholar 

  • Hourcade B, Perisse E, Devaud J-M, Sandoz J-C (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learn Mem 16:607–615

    Article  PubMed  Google Scholar 

  • Hourcade B, Muenz TS, Sandoz J-C, Rössler W, Devaud J-M (2010) Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain? J Neurosci 30:6461–6465

    Article  CAS  PubMed  Google Scholar 

  • Huetteroth W, Perisse E, Lin S, Klappenbach M, Burke C, Waddell S (2015) Sweet taste and nutrient value subdivide rewarding dopaminergic neurons in Drosophila. Curr Biol 25:751–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones BM, Leonard AS, Papaj DR, Gronenberg W (2013) Plasticity of the worker bumblebee brain in relation to age and rearing environment. Brain Behav Evol 82:250–261

    Article  PubMed  PubMed Central  Google Scholar 

  • Jorgensen K, Almaas TJ, Marion-Poll F, Mustaparta H (2007) Electrophysiological characterization of responses from gustatory receptor neurons of sensilla chaetica in the moth Heliothis virescens. Chem Senses 32:863–879

    Article  PubMed  Google Scholar 

  • Kandel E (2001) Neuroscience—the molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • Kromann SH, Saveer AM, Binyameen M, Bengtsson M, Birgersson G, Hansson BS, Schlyter F, Witzgall P, Ignell R, Becher PG (2015) Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth. Proc Biol Sci 282:20141884

    Article  PubMed  PubMed Central  Google Scholar 

  • Kvello P, Jorgensen K, Mustaparta H (2010) Central gustatory neurons integrate taste quality information from four appendages in the moth Heliothis virescens. J Neurophysiol 103:2965–2981

    Article  PubMed  Google Scholar 

  • Landgrebe M, Nyuyki K, Frank E, Steffens T, Hauser S, Eichhammer P, Hajak G, Langguth B (2008) Effects of colour exposure on auditory and somatosensory perception—hints for cross-modal plasticity. Neuro Endocrinol Lett 29:518–521

    PubMed  Google Scholar 

  • Liu C, Plaçais P-Y, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz I, Rubin GM, Preat T, Tanimoto H (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512–516

    Article  CAS  PubMed  Google Scholar 

  • Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62

    Article  CAS  PubMed  Google Scholar 

  • Minoli S, Kauer I, Colson V, Party V, Renou M, Anderson P, Gadenne C, Marion-Poll F, Anton S (2012) Brief exposure to sensory cues elicits stimulus-nonspecific general sensitization in an insect. PLoS ONE 7:e34141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfuhl G, Zhao XC, Ian E, Surlykke A, Berg BG (2014) Sound-sensitive neurons innervate the ventro-lateral protocerebrum of the heliothine moth brain. Cell Tissue Res 355:289–302

    Article  PubMed  Google Scholar 

  • Popescu A, Couton L, Almaas T-J, Rospars J-P, Wright GA, Marion-Poll F, Anton S (2013) Function and central projections of gustatory receptor neurons on the antenna of the noctuid moth Spodoptera littoralis. J Comp Physiol A 199:403–416

    Article  Google Scholar 

  • Sachse S, Rueckert E, Okada R, Tanaka N, Ito K, Vosshall LB (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56:838–850

    Article  CAS  PubMed  Google Scholar 

  • Saveer AM, Kromann SH, Birgersson G, Bengtsson M, Lindblom T, Balkenius A, Hansson BS, Witzgall P, Becher PG, Ignell R (2012) Floral to green: mating switches moth olfactory coding and preference. Proc Biol Sci 279:2314–2322

    Article  PubMed  PubMed Central  Google Scholar 

  • Scholl C, Wang Y, Krischke M, Mueller MJ, Amdam GV, Rössler W (2014) Light exposure leads to reorganization of microglomeruli in the mushroom bodies and influences juvenile hormone levels in the honeybee. Dev Neurobiol 74:1141–1153

    Article  CAS  PubMed  Google Scholar 

  • Schröter U, Menzel R (2003) A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. J Comp Neurol 465:168–178

    Article  PubMed  Google Scholar 

  • Stieb SM, Muenz TS, Wehner R, Rössler W (2010) Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis. Dev Neurobiol 70:408–423

    Article  PubMed  Google Scholar 

  • Yu L, Stein BE, Rowland BA (2009) Adult plasticity in multisensory neurons: short-term experience-dependent changes in the superior colliculus. J Neurosci 29:15910–15922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Fabien Tissier, Pascal Roskam and Jean-Christophe François for insect rearing.

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Correspondence to Sylvia Anton.

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This project was supported by the French National Funding Agency Grant ANR-07-Neuro-037-01.

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Anton, S., Chabaud, MA., Schmidt-Büsser, D. et al. Brief sensory experience differentially affects the volume of olfactory brain centres in a moth. Cell Tissue Res 364, 59–65 (2016). https://doi.org/10.1007/s00441-015-2299-0

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  • DOI: https://doi.org/10.1007/s00441-015-2299-0

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