Action of the noradrenergic system on adult-born cells is required for olfactory learning in mice

Journal of Neuroscience

Volumn 32, Issue 11, 2012, Pages 3748-3758

  Moreno, Melissa M ^a   Bath, Kevin ^b,c   Kuczewski, Nicola ^a   Sacquet, Joëlle ^a   Didier, Anne ^a   Mandairon, Nathalie ^a  

^a UNIVERSITÉ LYON 1   (France)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EFAROXAN; LABETALOL; NORADRENALIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HABITUATION; HISTOLOGY; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEWBORN; NONHUMAN; NORADRENERGIC SYSTEM; ODOR; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; TASK PERFORMANCE;

ADRENERGIC NEURONS; AGE FACTORS; ANIMALS; CELL SURVIVAL; LEARNING; MALE; MICE; MICE, INBRED C57BL; NEUROGENESIS; ODORS; OLFACTORY BULB; OLFACTORY PERCEPTION; RANDOM ALLOCATION;

EID: 84858042519     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6335-11.2012     Document Type: Article

References (43)

1. Alonso M, Viollet C, Gabellec MM, Meas-Yedid V, Olivo-Marin JC, Lledo PM (2006) Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci 26:10508-10513.
2. Bauer S, Moyse E, Jourdan F, Colpaert F, Martel JC, Marien M (2003) Effects of the alpha 2-adrenoreceptor antagonist dexefaroxan on neurogenesis in the olfactory bulb of the adult rat in vivo: selective protection against neuronal death. Neuroscience 117:281-291.
3. Bovetti S, Gribaudo S, Puche AC, De Marchis S, Fasolo A (2011) From progenitors to integrated neurons: role of neurotransmitters in adult olfactory neurogenesis. J Chem Neuroanat 42:304-316.
4. Brennan P, Kaba H, Keverne EB (1990) Olfactory recognition: a simple memory system. Science 250:1223-1226.
5. Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29:15245-15257.
6. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-518.
7. Cleland TA, Morse A, Yue EL, Linster C (2002) Behavioral models of odor similarity. Behav Neurosci 116:222-231.
8. Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354-8365.
9. Fletcher ML, Chen WR (2010) Neural correlates of olfactory learning: critical role of centrifugal neuromodulation. Learn Mem 17:561-570.
10. Gilbert CD, Sigman M, Crist RE (2001) The neural basis of perceptual learning. Neuron 31:681-697.
11. Gray CM, Freeman WJ, Skinner JE (1986) Chemical dependencies of learning in the rabbit olfactory bulb: acquisition of the transient spatial pattern change depends on norepinephrine. Behav Neurosci 100:585-596.
12. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153-1161.
13. Kermen F, Sultan S, Sacquet J, Mandairon N, Didier A (2010) Consolidation of an olfactory memory trace in the olfactory bulb is required for learning-induced survival of adult-born neurons and long-term memory. PLoS One 5:e12118.
14. Lazarini F, Mouthon MA, Gheusi G, de Chaumont F, Olivo-Marin JC, Lamarque S, Abrous DN, Boussin FD, Lledo PM (2009) Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 4:e7017.
15. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
16. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
17. Mandairon N, Jourdan F, Didier A (2003) Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119:507-516.
18. Mandairon N, Stack C, Kiselycznyk C, Linster C (2006a) Enrichment to odors improves olfactory discrimination in adult rats. Behav Neurosci 120:173-179.
19. Mandairon N, Sacquet J, Jourdan F, Didier A (2006b) Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: Influences of olfactory deprivation. Neuroscience 141:443-451.
20. Mandairon N, Stack C, Kiselycznyk C, Linster C (2006c) Broad activation of the olfactory bulb produces long-lasting changes in odor perception. Proc Natl Acad Sci U S A 103:13543-13548.
21. Mandairon N, Sacquet J, Garcia S, Ravel N, Jourdan F, Didier A (2006d) Neurogenic correlates of an olfactory discrimination task in the adult olfactory bulb. Eur J Neurosci 24:3578-3588.
22. Mandairon N, Peace S, Karnow A, Kim J, Ennis M, Linster C (2008a) Noradrenergic modulation in the olfactory bulb influences spontaneous and reward-motivated discrimination, but not the formation of habituation memory. Eur J Neurosci 27:1210-1219.
23. Mandairon N, Didier A, Linster C (2008b) Odor enrichment increases interneurons responsiveness in spatially defined regions of the olfactory bulb correlated with perception. Neurobiol Learn Mem 90:178-184.
24. Mandairon N, Sultan S, Nouvian M, Sacquet J, Didier A (2011) Involvement of newborn neurons in olfactory Associative learning? The operant or non-operant component of the task makes all the difference. J Neurosci 31:12455-12460.
25. Mayer P, Imbert T (2001) Alpha2-Adrenoreceptor antagonists. IDrugs 4:662-676.
26. McLean JH, Shipley MT, Nickell WT, Aston-Jones G, Reyher CK (1989) Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J Comp Neurol 285: 339-349.
27. Moreno MM, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009) Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci U S A 106:17980-17985.
28. Moriceau S, Sullivan RM (2004) Unique neural circuitry for neonatal olfactory learning. J Neurosci 24:1182-1189.
29. Mouly AM, Elaagouby A, Ravel N (1995) A study of the effects of noradrenaline in the rat olfactory bulb using evoked field potential response. Brain Res 681:47-57.
30. Nai Q, Dong HW, Linster C, Ennis M (2010) Activation of alpha1 and alpha2 noradrenergic receptors exert opposing effects on excitability of main olfactory bulb granule cells. Neuroscience 169:882-892.
31. Nissant A, Bardy C, Katagiri H, Murray K, Lledo PM (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12:728-730.
32. Palouzier-Paulignan B, Duchamp-Viret P, Hardy AB, Duchamp A (2002) GABA(B) receptor-mediated inhibition of mitral/tufted cell activity in the rat olfactory bulb: a whole-cell patch-clamp study in vitro. Neuroscience 111:241-250.
33. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-6113.
34. Rey NL, Sacquet J, Veyrac A, Jourdan F, Didier A (2012) Behavioral and cellular markers of olfactory aging and their response to enrichment. Neurobiol Aging 33:626.
35. Shea SD, Katz LC, Mooney R (2008) Noradrenergic induction of odorspecific neural habituation and olfactory memories. J Neurosci 28: 10711-10719.
36. Shipley MT, Halloran FJ, de la Torre J (1985) Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat. Brain Res 329:294-299.
37. Sullivan RM, Wilson DA (1994) The locus coeruleus, norepinephrine, and memory in newborns. Brain Res Bull 35:467-472.
38. Sullivan RM, Stackenwalt G, Nasr F, Lemon C, Wilson DA (2000) Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav Neurosci 114:957-962.
39. Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010) Learning-dependent neurogenesis in the olfactory bulb determines longterm olfactory memory. FASEB J 24:2355-2363.
40. Sultan S, Lefort JM, Sacquet J, Mandairon N, Didier A (2011) Acquisition of an olfactory associative task triggers a regionalized down-regulation of adult born neuron cell death. Front Neurosci 5:52.
41. Veyrac A, Nguyen V, Marien M, Didier A, Jourdan F (2007) Noradrenergic control of odor recognition in a nonassociative olfactory learning task in the mouse. Learn Mem 14:847-854.
42. Veyrac A, Sacquet J, Nguyen V, Marien M, Jourdan F, Didier A (2009) Novelty determines the effects of olfactory enrichment on memory and neurogenesis through noradrenergic mechanisms. Neuropsychopharmacology 34:786-795.
43. Wilson DA, Sullivan RM (1994) Neurobiology of associative learning in the neonate: early olfactory learning. Behav Neural Biol 61:1-18.