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Brain processing of a configural vs elemental odor mixture in the newborn rabbit

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Abstract

Organisms are surrounded throughout life by chemically complex odors. How individuals process an odorant within a mixture or a mixture as a whole is a key question in neuroethology and chemical senses. This question is addressed here by using newborn rabbits, which can be rapidly conditioned to a new stimulus by single association with the mammary pheromone. After conditioning to ethyl maltol (odorant B), pups behaviorally respond to B and an A′B′ mixture (68/32 ratio) but not to ethyl isobutyrate (odorant A) or an AB mixture (30/70 ratio). This suggests elemental and configural perception of A′B′ and AB, respectively. We then explored the neural substrates underlying the processing of these mixtures with the hypothesis that processing varies according to perception. Pups were pseudoconditioned or conditioned to B on postnatal day 3 before exposure to B, A′B′ or AB on day 4. Fos expression was not similar between groups (mainly in the olfactory bulb and posterior piriform cortex) suggesting a differential processing of the stimuli that might reflect either stimulus complexity or conditioning effect. Thus, the ratio of components in A′B′ vs AB leads to differential activation of the olfactory system which may contribute to elemental and configural percepts of these mixtures. In addition, together with recent behavioral data, this highlights that configural perception occurs even in relatively immature animals, emphasizing the value of the newborn rabbit for exploration of odor mixture processing from molecules to brain and behavior.

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References

  • Allingham K, Brennan PA, Distel H, Hudson R (1999) Expression of c-Fos in the main olfactory bulb of neonatal rabbits in response to garlic as a novel and conditioned odour. Behav Brain Res 104:157–167

    Article  CAS  PubMed  Google Scholar 

  • Barkat S, Le Berre E, Coureaud G, Sicard G, Thomas-Danguin T (2012) Perceptual blending in odor mixtures depends on the nature of odorants and human olfactory expertise. Chem Senses 37:159–166

    Article  CAS  PubMed  Google Scholar 

  • Barnes DC, Hofacer RD, Zaman AR, Rennaker RL, Wilson DA (2008) Olfactory perceptual stability and discrimination. Nat Neurosci 11:1378–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell GA, Laing DG, Panhuber H (1987) Odour mixture suppression: evidence for a peripheral mechanism in human and rat. Brain Res 426:8–18

    Article  CAS  PubMed  Google Scholar 

  • Boyd AM, Sturqill JF, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyle JA, Djordjevic J, Olsson MJ, Lundstrom JN, Jones-Gotman M (2009) The human brain distinguishes between single odorants and binary mixtures. Cereb Cortex 19:66–71

    Article  PubMed  Google Scholar 

  • Chapuis J, Wilson DA (2011) Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15:155–161

    Article  PubMed  PubMed Central  Google Scholar 

  • Charra R, Datiche F, Casthano A, Gigot V, Schaal B, Coureaud G (2012) Brain processing of the mammary pheromone in newborn rabbits. Behav Brain Res 226:179–188

    Article  CAS  PubMed  Google Scholar 

  • Charra R, Datiche F, Casthano A, Gigot V, Schaal B, Coureaud G (2013) Pheromone-induced odor learning modifies FOS expression in the newborn rabbit brain. Behav Brain Res 237:129–140

    Article  CAS  PubMed  Google Scholar 

  • Cleland TA (2010) Early transformations in odor representation. Trends Neurosci 33:130–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleland TA, Johnson BA, Leon M, Linster C (2007) Relational representation in the olfactory system. Proc Natl Acad Sci USA 104:1953–1958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coureaud G, Moncomble A, Montigny D, Dewas M, Perrier G, Schaal B (2006) A pheromone that rapidly promotes learning in the newborn. Curr Biol 16:1956–1961

    Article  CAS  PubMed  Google Scholar 

  • Coureaud G, Thomas-Danguin T, Le Berre E, Schaal B (2008) Perception of odor blending mixture in the newborn rabbit. Physiol Behav 95:194–199

    Article  CAS  PubMed  Google Scholar 

  • Coureaud G, Hamdani Y, Schaal B, Thomas-Danguin T (2009) Elemental and configural processing of odour mixtures in the newborn rabbit. J Exp Biol 212:2525–2531

    Article  PubMed  Google Scholar 

  • Coureaud G, Gibaud D, Le Berre E, Schaal B, Thomas-Danguin T (2011a) Proportion of odorants impacts the configural versus elemental perception of a binary blending mixture in newborn rabbits. Chem Senses 36:693–700

    Article  CAS  PubMed  Google Scholar 

  • Coureaud G, Languille S, Joly V, Schaal B, Hars B (2011b) Independence of first- and second-order memories in newborn rabbit. Learn Mem 18:401–404

    Article  PubMed  Google Scholar 

  • Coureaud G, Thomas-Danguin T, Wilson DA, Ferreira G (2014a) Neonatal representation of odour objects: distinct memories of the whole and its parts. Proc R Soc B 281:20133319

    Article  PubMed  PubMed Central  Google Scholar 

  • Coureaud G, Thomas-Danguin T, Datiche F, Wilson DA, Ferreira G (2014b) Differential memory persistence of odour mixture and components in newborn rabbits: competition between the whole and its parts. Front Behav Neurosci 8:211

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Deisig N, Giurfa M, Sandoz JC (2010) Antennal lobe processing increases separability of odor mixture representations in the honeybee. J Neurophysiol 103:2185–2194

    Article  PubMed  Google Scholar 

  • Derby CD, Hutson M, Andrew Livermore B, Lynn WH (1996) Generalization among related complex odorant mixtures and their components: analysis of olfactory perception in the spiny lobster. Physiol Behav 60:87–95

    Article  CAS  PubMed  Google Scholar 

  • Doucette W, Restrepo D (2008) Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol 6:e258

    Article  PubMed  PubMed Central  Google Scholar 

  • Duchamp-Viret P, Duchamp A, Chaput MA (2003) Single olfactory sensory neurons simultaneously integrate the components of an odour mixture. Eur J Neurosci 18:2690–2696

    Article  PubMed  Google Scholar 

  • Dulac C (2006) Sparse encoding of natural scents. Neuron 50:816–818

    Article  CAS  PubMed  Google Scholar 

  • Fletcher ML (2011) Analytical processing of binary mixture information by olfactory bulb glomeruli. PLoS One 6:e29360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fletcher ML, Bendahmane M (2014) Visualizing olfactory learning functional imaging of experience-induced olfactory bulb changes. Prog Brain Res 208:89–113

    Article  PubMed  Google Scholar 

  • Fletcher ML, Chen WR (2010) Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learn Mem 17:561–570

    Article  PubMed  PubMed Central  Google Scholar 

  • Giessel AJ, Datta SR (2014) Olfactory maps, circuits and computations. Curr Opin Neurobiol 24:120–132

    Article  CAS  PubMed  Google Scholar 

  • Gottfried JA (2009) Function follows form: ecological constraints on odor codes and olfactory percepts. Curr Opin Neurobiol 19:422–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11:628–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grossman KJ, Mallik AK, Ross J, Kay LM, Issa NP (2008) Glomerular activation patterns and the perception of odor mixtures. Eur J Neuosci 27:2676–2685

    Article  Google Scholar 

  • Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576

    Article  CAS  PubMed  Google Scholar 

  • Jagalska-Majewska H, Luczynska A, Wojcik S, Dziewiatkowski J, Kurlapska R, Morys J (2003) Developmental changes of morphology in the basolateral complex of the rabbit amygdala. Folia Morphol 62:227–230

    Google Scholar 

  • Johnson BA, Leon M (2007) Chemotopic odorant coding in a mammalian olfactory system. J Comp Neurol 503:1–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadohisa M, Wilson DA (2006) Separate encoding of identity and similarity of complex familiar odors in piriform cortex. PNAS 103:15206–15211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay LM, Lowry CA, Jacobs HA (2003) Receptor contributions to configural and elemental odor mixture perception. Behav Neurosci 117:1108–1114

    Article  PubMed  Google Scholar 

  • Kay LM, Crk T, Thorngate J (2005) A redefinition of odor mixture quality. Behav Neurosci 119:726–733

    Article  CAS  PubMed  Google Scholar 

  • Knafo S, Grossman Y, Barkai E, Benshalom G (2001) Olfactory learning is associated with increased spine density along apical dendrites of pyramidal neurons in the rat piriform cortex. Eur J Neurosci 13:633–638

    Article  CAS  PubMed  Google Scholar 

  • Laing DG, Francis GW (1989) The capacity of humans to identify odors in mixtures. Physiol Behav 46:809–814

    Article  CAS  PubMed  Google Scholar 

  • Le Berre E, Thomas-Danguin T, Béne N, Coureaud G, Etievant P, Prescott J (2008) Perceptual processing strategy and exposure influence the perception of odor mixtures. Chem Senses 33:193–199

    Article  PubMed  Google Scholar 

  • Linster C, Cleland TA (2004) Configurational and elemental odor mixture perception can arise from local inhibition. J Comp Neurosci 16:39–47

    Article  Google Scholar 

  • Linster C, Johnson BA, Yue E, Morse A, Xu Z, Hingco EE, Choi Y, Choi M, Messiha A, Leeon M (2001) Perceptual correlates of neural representations evoked by odorant enantiomers. J Neurosci 21:9837–9843

    CAS  PubMed  Google Scholar 

  • Litaudon P, Mouly AM, Sullivan R, Gervais R, Cattarelli M (1997) Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur J Neurosci 9:1593–1602

    Article  CAS  PubMed  Google Scholar 

  • Martin JP, Lei H, Riffell JA, Hildebrand JG (2013) Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta. J Comp Physiol A 199:963–979

    Article  CAS  Google Scholar 

  • Matsutani S (2010) Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience 169:436–448

    Article  CAS  PubMed  Google Scholar 

  • Montigny D, Coureaud G, Schaal B (2006) Rabbit pup response to the mammary pheromone: from automatism to prandial control. Physiol Behav 89:742–749

    Article  CAS  PubMed  Google Scholar 

  • Oka Y, Omura M, Kataoka H, Touhara K (2004) Olfactory receptor antagonism between odorants. EMBO J 23:120–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press Inc, London

    Google Scholar 

  • Restrepo D, Doucette W, Whitesell JD, McTavish TS, Salcedo E (2009) From the top down: flexible reading of a fragmental odor map. Trends Neurosci 32:525–531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riffell JA (2012) Olfactory ecology and the processing of complex mixtures. Curr Opin Neurobiol 22:236–242

    Article  CAS  PubMed  Google Scholar 

  • Salcedo E, Zhang C, Kronberg E, Restrepo D (2005) Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. Chem Senses 30:615–626

    Article  CAS  PubMed  Google Scholar 

  • Shek JW, Wen GY, Wisniewski HM (1986) Atlas of the rabbit brain and spinal cord. Karger, Staten Island

    Google Scholar 

  • Sinding C, Thomas-Danguin T, Crepeaux G, Schaal B, Coureaud G (2011) Experience influences elemental and configural perception of certain binary odour mixtures in newborn rabbits. J Exp Biol 214:4171–4178

    Article  CAS  PubMed  Google Scholar 

  • Spors H, Albeanu DF, Murthy VN, Rinberg D, Naoshige Uchida, Wachowiak M, Friedrich RW (2012) Illuminating vertebrate olfactory processing. J Neurosci 32:14102–14108a

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terleph TA, Tremere LA (2006) The use of immediate early genes as mapping tools for neuronal activation: concepts and methods. In: Pinaud R, Tremere LA (eds) Immediate early genes in sensory processing, cognitive performance and neurological disorders. Springer, New York, pp 1–10

    Chapter  Google Scholar 

  • Thomas-Danguin T, Le Berre E, Barkat S, Coureaud G, Sicard G (2007) Evidence for odor blending in odorant mixtures. Chem Annu Meet 32:A64

    Article  Google Scholar 

  • Thomas-Danguin T, Sinding C, Romagny S, El Mountassir F, Atanasova B, Le Berre E, Le Bon A-M, Coureaud G (2014) The perception of odor objects in everyday life: a review on the processing of odor mixtures. Front Psychol 5:1–18

    Article  Google Scholar 

  • Vassar R, Chao SK, Sitcheran R, Nuñez JM, Vosshall LB, Axel R (1994) Topographic organization of sensory projections to the olfactory bulb. Cell 79:981–991

    Article  CAS  PubMed  Google Scholar 

  • Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarrow MX, Denenberg VH, Anderson CO (1965) Rabbit: frequency of suckling in the pup. Science 150:1835–1836

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We sincerely thank Valérie Saint-Giorgio, Nicolas Malaty and Florent Costilhes (Centre de Zootechnie, Dijon) as well as Camille Royer, Paul Jeanneau and Martin Saïdi for their technical assistance. The work was supported by the French Agence Nationale de la Recherche (ANR-2010-JCJC-1410-1 MEMOLAP grant) and pôle VITAGORA.

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The authors declare that they have no conflict of interest.

Ethical standard

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed were covered by ethical committee authorization no. 1608 from the University of Burgundy and no. 01273.01 from the French Ministry of Higher Education and Research.

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This article does not contain any studies with human participants performed by any of the authors.

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Correspondence to Nanette Y. Schneider or Gérard Coureaud.

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Schneider, N.Y., Datiche, F., Wilson, D.A. et al. Brain processing of a configural vs elemental odor mixture in the newborn rabbit. Brain Struct Funct 221, 2527–2539 (2016). https://doi.org/10.1007/s00429-015-1055-2

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