Pheromone-induced odor learning modifies Fos expression in the newborn rabbit brain

Behavioural Brain Research

Volumn 237, Issue 1, 2013, Pages 129-140

  Charra, R ^a   Datiche, F ^a   Gigot, V ^a   Schaal, B ^a   Coureaud, G ^a  

^a CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

Amygdala; C fos; Lateral preoptic area; Learning; Main olfactory system; Mammary pheromone; Newborn; Piriform cortex; Rabbit

Indexed keywords

ACETOACETIC ACID; ETHYL ACETOACETIC ACID; PHEROMONE; PROTEIN FOS; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN MAPPING; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; INSTRUMENTAL CONDITIONING; MALE; MITRAL CELL; MOLECULAR DYNAMICS; NEWBORN; NONHUMAN; ODOR; OLFACTORY BULB; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRIFORM CORTEX; RABBIT; SMELLING; STATE DEPENDENT LEARNING; SUCKING;

ANIMALS; ANIMALS, NEWBORN; ASSOCIATION LEARNING; BRAIN; BRAIN MAPPING; CELL COUNT; ODORS; ONCOGENE PROTEINS V-FOS; PHEROMONES; RABBITS; SUCKING BEHAVIOR;

EID: 84867120359     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.09.017     Document Type: Article

References (84)

1. Gottlieb G. The roles of experience in the development of behavior and the nervous system. Neural and behavioral specificity 1976, 25-54. Academic Press, New York. G. Gottlieb (Ed.).
2. Alberts J.R. Learning as adaptation of the infant. Acta Paediatrica. Supplement 1994, 397:77-85.
3. Bolhuis J. Development of perceptual mechanisms in birds: predispositions and imprinting 1996, 158-184. Westview Press, Boulder (Colorado). C.F. Moss, S.J. Shettleworth (Eds.).
4. Slater A., Kirby R. Innate and learned perceptual abilities in the newborn infant. Experimental Brain Research 1998, 123:90-94.
5. Miller S.S., Spear N.E. Olfactory learning in the rat immediately after birth: Unique salience of first odors. Developmental Psychobiology 2009, 51:488-504.
6. Teicher M.H., Blass E.M. First suckling response of the newborn albino rat: the roles of olfaction and amniotic fluid. Science 1977, 198:635-636.
7. Schaal B., Marlier L., Soussignan R. Human foetuses learn odours from their pregnant mother's diet. Chemical Senses 2000, 25:729-737.
8. Smotherman W.P., Robinson S.R., La Vallee P.A., Hennessy M.B. Influences of the early olfactory environment on the survival, behavior and pituitary-adrenal activity of caesarean delivered preterm rat pups. Developmental Psychobiology 1987, 20:415-423.
9. Johanson I.B., Hall W.G. Appetitive learning in 1-day-old rat pups. Science 1979, 205:419-421.
10. Brake S.C. Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery. Science 1981, 211:506-508.
11. Johanson I.B., Hall W.G., Polefrone J.M. Appetitive conditioning in neonatal rats: conditioned ingestive responding to stimuli paired with oral infusions of milk. Developmental Psychobiology 1984, 17:357-381.
12. Sullivan R.M., Hofer M.A., Brake S.C. Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state. Developmental Psychobiology 1986, 19:615-623.
13. Sevelinges Y., Lévy F., Mouly A.M., Ferreira G. Rearing with artificially scented mothers attenuates conditioned odor aversion in adulthood but not its amygdala dependency. Behavioural Brain Research 2009, 198:313-320.
14. Coopersmith R., Leon M. Enhanced neural response to familiar olfactory cues. Science 1984, 225:849-851.
15. Sullivan R.M., Wilson D.A. Molecular biology of early olfactory memory. Learning and Memory 2003, 10:1-4.
16. Best A.R., Wilson D.A. A postnatal sensitive period for plasticity of cortical afferents but not cortical association fibers in rat piriform cortex. Brain Research 2003, 961:81-87.
17. Kerr M.A., Belluscio L. Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nature Neuroscience 2006, 9:484-486.
18. Sullivan R.M., Wilson D.A., Wong R., Correa A., Leon M. Modified behavioral and olfactory bulb responses to maternal odors in preweanling rats. Developmental Brain Research 1990, 53:243-247.
19. Roth T.L., Sullivan R.M. Memory of early maltreatment: neonatal behavioral and neural correlates of maternal maltreatment within the context of classical conditioning. Biological Psychiatry 2005, 57:823-831.
20. Johnson B.A., Woo C.C., Duong H., Nguyen V., Leon M. A learned odor evokes an enhanced fos-like glomerular response in the olfactory bulb of young rats. Brain Research 1995, 699:192-200.
21. Wilson D.A., Leon M. Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. Journal of Neurophysiology 1988, 59:1770-1782.
22. Fletcher M.L., Chen W.R. Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learning and Memory 2010, 17:561-570.
23. Sullivan R.M., Wilson D.A. Role of the amygdala complex in early olfactory associative learning. Behavioral Neuroscience 1993, 107:254-263.
24. Litaudon P., Mouly A.M., Sullivan R., Gervais R., Cattarelli M. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. European Journal of Neuroscience 1997, 9:1593-1602.
25. Knafo S., Grossman Y., Barkai E., Benshalom G. Olfactory learning is associated with increased spine density along apical dendrites of pyramidal neurons in the rat piriform cortex. European Journal of Neuroscience 2001, 13:633-638.
26. Bilkó A., Altbäcker V., Hudson R. Transmission of food preference in the rabbit: the means of information transfer. Physiology and Behavior 1994, 56:907-912.
27. Altbäcker V., Hudson R., Bilkó A. Rabbit mothers' diet influences pups' later food. Ethology 1995, 99:107-116.
28. Coureaud G., Schaal B., Hudson R., Orgeur P., Coudert P. Transnatal olfactory continuity in the rabbit: behavioral evidence and short-term consequence of its disruption. Developmental Psychobiology 2002, 40:372-390.
29. Ivanitskii A.M. The morphological investigation of development of conditioned alimentary reaction in rabbits during ontogenesis. Experimental studies of higher nervous activity in man and animals. Israel Program for Scientific Translation, Jerusalem 1962, 126-141.
30. Hudson R. Do newborn rabbits learn the odor stimuli releasing nipple-search behavior?. Developmental Psychobiology 1985, 18:575-585.
31. Kindermann U., Hudson R., Distel H. Learning of suckling odors by newborn rabbits declines with age and suckling experience. Developmental Psychobiology 1994, 27:111-122.
32. Serra J., Nowak R. Olfactory preference for own mother and litter in 1-day-old rabbits and its impairment by thermotaxis. Developmental Psychobiology 2008, 50:542-553.
33. Semke E., Distel H., Hudson R. Specific enhancement of olfactory receptor sensitivity associated with foetal learning of food odors in the rabbit. Naturwissenschaften 1995, 82:148-149.
34. Allingham K., Brennan P.A., Distel H., Hudson R. Expression of c-fos in the main olfactory bulb of neonatal rabbits in response to garlic as a novel and conditioned odour. Behavioural Brain Research 1999, 104:157-167.
35. Zarrow M.X., Denenberg V.H., Anderson C.O. Rabbit: frequency of suckling in the pup. Science 1965, 150:1835-1836.
36. Beauchamp G.K., Doty R.L., Moulton D.G., Mugford R.A. The pheromone concept in mammals: a critique. Mammalian olfaction, reproductive processes, and behavior 1976, 143-160. Academic Press, New York. R.L. Doty (Ed.).
37. Coureaud G. Olfactory regulation of sucking in newborn rabbit: ethological and chemical characterization of a pheromonal signal. Doctoral Thesis, University Paris 13; 2001.
38. Coureaud G., Langlois D., Perrier G., Schaal B. A single key-odorant accounts for the pheromonal effect of rabbit milk: further test of the mammary pheromone's activity against a wide sample of volatiles from milk. Chemoecology 2003, 13:187-192.
39. Schaal B., Coureaud G., Langlois D., Giniès C., Sémon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 2003, 424:68-72.
40. Coureaud G., Moncomble A., Montigny D., Dewas M., Perrier G., Schaal B. A pheromone that rapidly promotes learning in the newborn. Current Biology 2006, 16:1956-1961.
41. Coureaud G., Thomas-Danguin T., Le Berre E., Schaal B. Perception of odor blending mixtures in the newborn rabbit. Physiology and Behavior 2008, 95:194-199.
42. Coureaud G., Languille S., Schaal B., Hars B. Pheromone-induced olfactory memory in newborn rabbits: involvement of consolidation and reconsolidation processes. Learning and Memory 2009, 16:470-473.
43. Coureaud G., Gibaud D., Le Berre E., Schaal B., Thomas-Danguin T. Proportion of odorants impacts the configural versus elemental perception of a blending mixture in newborn rabbits. Chemical Senses 2011, 36:693-700.
44. Coureaud G., Charra R., Datiche F., Sinding C., Thomas-Danguin T., Languille S., Hars B., Schaal B. A pheromone to behave, a pheromone to learn: the rabbit mammary pheromone. Journal of Comparative Physiology 2010, 196:779-790.
45. Charra R., Datiche F., Casthano A., Gigot V., Schaal B., Coureaud G. Brain processing of the mammary pheromone in newborn rabbits. Behavioural Brain Research 2012, 226:179-188.
46. Gall C.M., Hess U.S., Lynch G. Mapping brain networks engaged by, and changed by, learning. Neurobiology of Learning and Memory 1998, 70:14-36.
47. Montigny D., Coureaud G., Schaal B. Rabbit pup response to the mammary pheromone: from automatism to prandial control. Physiology and Behavior 2006, 89:742-749.
48. Girgis M., Shih-Chang W. A new stereotaxic atlas of the rabbit brain 1981, Warren H Green Inc., Saint Louis.
49. Jagalska-Majewska H., Luczyńska A., Wójcik S., Dziewiatkowski J., Kurlapska R., Moryś J. Developmental changes of morphology in the basolateral complex of the rabbit amygdala. Folia Morphologiica 2003, 62:227-230.
50. Teicher M.H., Stewart W.B., Kauer J.S., Shepherd G.M. Suckling pheromone stimulation of a modified glomerular region in the developing rat olfactory bulb revealed by the 2-deoxyglucose method. Brain Research 1980, 194:530-535.
51. Freeman W.J., Schneider W. Changes in spatial patterns of rabbit olfactory eeg with conditioning to odors. Psychophysiology 1982, 19:44-56.
52. Solov'eva N.A., Lagutina L.V., Antonova L.V., Anokhin K.V. Regulation of c-fos gene expression in the rat olfactory bulb during olfactory learning. Neuroscience and Behavioral Physiology 2007, 37:697-704.
53. Johnson B.A., Leon M. Chemotopic odorant coding in a mammalian olfactory system. Journal of Comparative Neurology 2007, 503:1-34.
54. Busto G.U., Elie J.E., Kermen F., Garcia S., Sacquet J., Jourdan F., Marcel D., Mandairon N., Didier A. Expression of Zif268 in the granule cell layer of the adult mouse olfactory bulb is modulated by experience. European Journal of Neuroscience 2009, 29:1431-1439.
55. Doucette W., Gire D.H., Whitesell J., Carmean V., Lucero M.T., Restrepo D. Associative cortex features in the first olfactory brain relay station. Neuron 2011, 69:1176-1187.
56. Coureaud G., Languille S., Joly V., Schaal B., Hars B. Independence of first- and second-order memories in newborn rabbits. Learning and Memory 2011, 18:401-404.
57. Matsutani S. Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience 2010, 169:436-448.
58. Pressler R.T., Inoue T., Strowbridge B.W. Muscarinic receptor activation modulates granule cell excitability and potentiates inhibition onto mitral cells in the rat olfactory bulb. Journal of Neuroscience 2007, 27:10969-10981.
59. Illig K.R. Developmental changes in odor-evoked activity in rat piriform cortex. Neuroscience 2007, 145:370-376.
60. Choi G.B., Stettler D.D., Kallman B.R., Bhaskar S.T., Fleischmann A., Axel R. Driving opposing behaviors with ensembles of piriform neurons. Cell 2011, 146:1004-1015.
61. Datiche F., Litaudon P., Cattarelli M. Intrinsic association fiber system of the piriform cortex: a quantitative study based on a cholera toxin b subunit tracing in the rat. Journal of Comparative Neurology 1996, 376:265-277.
62. Haberly L.B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chemical Senses 2001, 26:551-576.
63. Franks K.M., Russo M.J., Sosulski D.L., Mulligan A.A., Siegelbaum S.A., Axel R. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 2011, 72:49-56.
64. Zinyuk L.E., Datiche F., Cattarelli M. Cell activity in the anterior piriform cortex during an olfactory learning in the rat. Behavioural Brain Research 2001, 124:29-32.
65. Roesch M.R., Stalnaker T.A., Schoenbaum G. Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning. Cerebral Cortex 2007, 17:643-652.
66. Calu D.J., Roesch M.R., Stalnaker T.A., Schoenbaum G. Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cerebral Cortex 2007, 17:1342-1349.
67. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 2002, 26:321-352.
68. Everitt B.J., Cardinal R.N., Parkinson J.A., Robbins T.W. Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Annals of the New York Academy of Sciences 2003, 985:233-250.
69. Broadwell R.D. Olfactory relationships of the telencephalon and diencephalon in the rabbit. I. An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs. Journal of Comparative Neurology 1975, 163:329-345.
70. McDonald A.J. Cortical pathways to the mammalian amygdala. Progress in Neurobiology 1998, 55:257-332.
71. Petrovich G.D., Gallagher M. Amygdala subsystems and control of feeding behavior by learned cues. Annals of the New York Academy of Sciences 2003, 985:251-262.
72. Majak K., Rönkkö S., Kemppainen S., Pitkänen A. Projections from the amygdaloid complex to the piriform cortex: a pha-l study in the rat. Journal of Comparative Neurology 2004, 476:414-428.
73. Hegoburu C., Sevelinges Y., Thévenet M., Gervais R., Parrot S., Mouly A. Differential dynamics of amino acid release in the amygdala and olfactory cortex during odor fear acquisition as revealed with simultaneous high temporal resolution microdialysis. Learning and Memory 2009, 16:687-697.
74. Sevelinges Y., Gervais R., Messaoudi B., Granjon L., Mouly A.M. Olfactory fear conditioning induces field potential potentiation in rat olfactory cortex and amygdala. Learning and Memory 2004, 11:761-769.
75. Scalia F. Some olfactory pathways in the rabbit brain. Journal of Comparative Neurology 1966, 126:285-310.
76. Osaka T., Ueta Y., Yamashita H. Activity of neurons in the lateral preoptic area during drinking behavior by the rat. Brain Research Bulletin 1995, 36:361-369.
77. Ono T., Nakamura K. Learning and integration of rewarding and aversive stimuli in the rat lateral hypothalamus. Brain Research 1985, 346:368-373.
78. Cragg B.G. The connections of the habenula in the rabbit. Experimental Neurology 1961, 3:388-409.
79. Kowski A.B., Geisler S., Krauss M., Veh R.W. Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. Journal of Comparative Neurology 2008, 507:1465-1478.
80. Ikemoto S. Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neuroscience and Biobehavioral Reviews 2010, 35:129-150.
81. Paul M.J., Indic P., Schwartz W.J. A role for the habenula in the regulation of locomotor activity cycles. European Journal of Neuroscience 2011, 34:478-488.
82. Allingham K., von Saldern C., Brennan P.A., Distel H., Hudson R. Endogenous expression of C-Fos in hypothalamic nuclei of neonatal rabbits coincides with their circadian pattern of suckling-associated arousal. Brain Research 1998, 783:210-218.
83. Choi D.L., Davis J.F., Magrisso I.J., Fitzgerald M.E., Lipton J.W., Benoit S.C. Orexin signaling in the paraventricular thalamic nucleus modulates mesolimbic dopamine and hedonic feeding in the rat. Neuroscience 2012, 210:243-248.
84. Nakahara K., Fukui K., Murakami N. Involvement of thalamic paraventricular nucleus in the anticipatory reaction under food restriction in the rat. Journal of Veterinary Medical Science 2004, 66:1297-1300.