Enhanced synaptic integration of adult-born neurons in the olfactory bulb of lactating mothers

Journal of Neuroscience

Volumn 32, Issue 22, 2012, Pages 7519-7527

  Kopel, Hagit ^a,b   Schechtman, Eitan ^b   Groysman, Maya ^a,b   Mizrahi, Adi ^a,b  

^a Institute of Life Sciences   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; GRANULE CELL; HISTOLOGY; HUMAN; HUMAN CELL; LACTATION; MATERNAL BEHAVIOR; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; STEM CELL NICHE; SYNAPTIC TRANSMISSION; TIME LAPSE IMAGING;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; DENDRITIC SPINES; FEMALE; GENE EXPRESSION REGULATION; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; LACTATION; MALE; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEURONAL PLASTICITY; NEURONS; OLFACTORY BULB; PREGNANCY; STATISTICS, NONPARAMETRIC; STEM CELL NICHE; SYNAPSES; SYNAPTOPHYSIN; TRANSDUCTION, GENETIC;

EID: 84861619975     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6354-11.2012     Document Type: Article

References (85)

1. Abraham NM, Egger V, Shimshek DR, Renden R, Fukunaga I, Sprengel R, Seeburg PH, Klugmann M, Margrie TW, Schaefer AT, Kuner T (2010) Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65:399-411.
2. Adam Y, Mizrahi A (2011) Long-term imaging reveals dynamic changes inthe neuronal composition of the glomerular layer. J Neurosci 31:7967-7973.
3. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433-457.
4. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
5. Alvarez VA, Sabatini BL (2007) Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 30:79-97.
6. Baum MJ, Kelliher KR (2009) Complementary roles of the main and accessory olfactory systems in mammalian mate recognition. Annu Rev Physiol 71:141-160.
7. Bhatt DH, Zhang S, Gan WB (2009) Dendritic spine dynamics. Annu Rev Physiol 71:261-282.
8. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 361:2061-2078.
9. Brennan PA, Kendrick KM, Keverne EB (1995) Neurotransmitter release in the accessory olfactory bulb during and after the formation of an olfactory memory in mice. Neuroscience 69:1075-1086.
10. Brennan PA, Schellinck HM, de la Riva C, Kendrick KM, Keverne EB (1998) Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice. Neuroscience 87:583-590.
11. Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Inter neurons 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.
12. Brock O, Keller M, Veyrac A, Douhard Q, Bakker J (2010) Short term treatment with estradiol decreases the rate of newly generated cells in the sub ventricular zone and main olfactory bulb of adult female mice. Neuroscience 166:368-376.
13. Brunton PJ, Russell JA (2008) The expectant brain: adapting for motherhood. Nat Rev Neurosci 9:11-25.
14. 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.
15. Carter CS, Altemus M, Chrousos GP (2001) Neuroendocrine and emotional changes in the post-partum period. Prog Brain Res 133:241-249.
16. Cohen L, Rothschild G, Mizrahi A (2011) Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72:357-369.
17. Dahlen JE, Jimenez DA, Gerkin RC, Urban NN (2011) Morphological analysis of activity-reduced adult-born neurons in the mouse olfactory bulb. Front Neurosci 5:66.
18. Dickinson C, Keverne EB (1988) Importance of noradrenergic mechanisms in the olfactory bulbs for the maternal behaviour of mice. Physiol Behav 43:313-316.
19. Feierstein CE, Lazarini F, Wagner S, Gabellec MM, de Chaumont F, Olivo- Marin JC, Boussin FD, Lledo PM, Gheusi G (2010) Disruption of adult neuro genesis in the olfactory bulb affects social interaction but not maternal behavior. Front Behav Neurosci 4:176.
20. Furuta M, Bridges RS (2005) Gestation-induced cell proliferation in the rat brain. Brain Res Dev Brain Res 156:61-66.
21. Galindo-Leon EE, Lin FG, Liu RC (2009) Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 62:705-716.
22. Gandelman R, Zarrow MX, Denenberg VH, Myers M (1971) Olfactory bulb removal eliminates maternal behavior in the mouse. Science 171:210-211.
23. Gao Y, Strowbridge BW (2009) Long-term plasticity of excitatory inputs to granule cells in the rat olfactory bulb. Nat Neurosci 12:731-733.
24. Gross CG (2000) Neuro genesis in the adult brain: death of a dogma. Nat Rev Neurosci 1:67-73.
25. Grota LJ, Ader R (1969) Continuous recording of maternal behaviour in Rattus norvegicus. Animal Behav 17:722-729.
26. Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 457:313-338.
27. Guéneau G, Privat A, Drouet J, Court L (1982) Sub granular zone of the dentate gyrus of young rabbits as a secondary matrix. A high-resolution autoradiographic study. Dev Neurosci 5:345-358.
28. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457:313-317.
29. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647-658.
30. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45: 279-291.
31. Holtmaat A, Bonhoeffer T, Chow DK, Chuckowree J, De Paola V, Hofer SB, Hübener M, Keck T, Knott G, Lee WC, Mostany R, Mrsic-Flogel TD, Nedivi E, Portera-Cailliau C, Svoboda K, Trachtenberg JT, Wilbrecht L (2009) Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4:1128-1144.
32. Hubener M, Bonhoeffer T (2010) Searching for engrams. Neuron 67: 363-371.
33. Isaacson JS, Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749-761.
34. Jahr CE, Nicoll RA (1980) Dendrodendritic inhibition: demonstration with intracellular recording. Science 207:1473-1475.
35. Keller M, Baum MJ, Brock O, Brennan PA, Bakker J (2009) The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav Brain Res 200:268-276.
36. Kelsch W, Lin CW, Lois C (2008) Sequential development of synapses in dendritic domains during adult neurogenesis. Proc Natl Acad Sci U S A 105:16803-16808.
37. Kelsch W, Lin CW, Mosley CP, Lois C (2009) A critical period for activitydependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 29:11852-11858.
38. Kendrick KM, Lévy F, Keverne EB (1992) Changes in the sensory processing of olfactory signals induced by birth in sleep. Science 256: 833-836.
39. Kendrick KM, Guevara-Guzman R, Zorrilla J, Hinton MR, Broad KD, Mimmack M, Ohkura S (1997) Formation of olfactory memories mediated by nitric oxide. Nature 388:670-674.
40. Kinsley CH, Trainer R, Stafisso-Sandoz G, Quadros P, Marcus LK, Hearon C, Meyer EA, Hester N, Morgan M, Kozub FJ, Lambert KG (2006) Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm Behav 49:131-142.
41. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26: 2000-2009.
42. Larsen CM, Grattan DR (2010) Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 151:3805-3814.
43. Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263-297.
44. Lazarini F, Lledo PM (2011) Is adult neurogenesis essential for olfaction? Trends Neurosci 34: 20-30.
45. Leuner B, Gould E (2010) Dendritic growth in medial prefrontal cortex and cognitive flexibility are enhanced during the postpartum period. J Neurosci 30: 13499-13503.
46. Leuner B, Glasper ER, Gould E (2010) Parenting and plasticity. Trends Neurosci 33:465- 473.
47. Lévy F, Gervais R, Kindermann U, Orgeur P, Piketty V (1990) Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav Neurosci 104:464-469.
48. Lévy F, Gheusi G, Keller M (2011) Plasticity of the parental brain: a case for neurogenesis. J Neuroendocrinol 23: 984-993.
49. Lin CW, Sim S, Ainsworth A, Okada M, Kelsch W, Lois C (2010) Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65:32-39.
50. Liu RC, Linden JF, Schreiner CE (2006) Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J Neurosci 23:3087-3097.
51. Livneh Y, Mizrahi A (2011) Long-term changes in the morphology and synaptic distributions of adult-born neurons. J Comp Neurol 519:2212-2224.
52. Livneh Y, Mizrahi A (2012) Experience-dependent plasticity of mature adult-born neurons. Nat Neurosci 15: 26-28.
53. Livneh Y, Feinstein N, Klein M, Mizrahi A (2009) Sensory input enhances synaptogenesis of adult-born neurons. J Neurosci 29:86-97.
54. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
55. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
56. Mann PE, Bridges RS (2001) Lactogenic hormone regulation of maternal behavior. Prog Brain Res 133:251-262.
57. Margrie TW, Sakmann B, Urban NN (2001) Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc Natl Acad Sci U S A 98:319-324.
58. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
59. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
60. Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10:444-452.
61. Mizrahi A, Katz LC (2003) Dendritic stability in the adult olfactory bulb. Nat Neurosci 6:1201-1207.
62. Mori K, Takagi SF (1978) An intracellular study of dendrodendritic inhibitory synapses on mitral cells in the rabbit olfactory bulb. J Physiol 279:569-588.
63. Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711-715.
64. Noirot E (1969) Serial order of maternal responses in mice. Anim Behav 17:547-550.
65. Noirot E (1972) Ultrasounds and maternal behavior in small rodents. Dev Psychobiol 5:371-387.
66. Nusser Z, Kay LM, Laurent G, Homanics GE, Mody I (2001) Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86:2823-2833.
67. Pawluski JL, Galea LA (2006) Hippocampal morphology is differentially affected by reproductive experience in the mother. J Neurobiol 66:71- 81.
68. Pawluski JL, Barakauskas VE, Galea LA (2010) Pregnancy decreases oestrogen receptor alpha expression and pyknosis, but not cell proliferation or survival, in the hippocampus. J Neuroendocrinol 22:248-257.
69. Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22:6106-6113.
70. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232:232-235.
71. Roberts TF, Tschida KA, Klein ME, Mooney R (2010) Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 463:948-952.
72. Rochefort C, Gheusi G, Vincent JD, Lledo PM (2002) Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679-2689.
73. Saghatelyan A, Roux P, Migliore M, Rochefort C, Desmaisons D, Charneau P, Shepherd GM, Lledo PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103-116.
74. Sakamoto M, Imayoshi I, Ohtsuka T, Yamaguchi M, Mori K, Kageyama R (2011) Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci U S A 108:8479-8484.
75. Schaefer ML, Yamazaki K, Osada K, Restrepo D, Beauchamp GK (2002) Olfactory fingerprints for major histocompatibility complex-determined body odors II: relationship among odor maps, genetics, odor composition, and behavior. J Neurosci 22:9513-9521.
76. Seitz PF (1958) The maternal instinct in animal subjects. I. Psychosom Med 20:215-226.
77. Shepherd G, Chen WI, Greer CA (2004) Olfactory bulb. In: The synaptic organization of the brain (Shepherd G, ed), pp 165-216. Oxford, UK: Oxford UP.
78. Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross JC, Weiss S (2003) Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299:117-120.
79. Urban NN (2002) Lateral inhibition in the olfactory bulb and in olfaction. Physiol Behav 77:607-612.
80. Urban NN, Arevian AC (2009) Computing with dendrodendritic synapses in the olfactory bulb. Ann N Y Acad Sci 1170:264-269.
81. Vandenbergh JG (1973) Effects of central and peripheral anosmia on reproduction of female mice. Physiol Behav 10:257-261.
82. Whitman MC, Greer CA (2007) Synaptic integration of adult-generated olfactory bulb granule cells: basal axodendritic centrifugal input precedes apical dendrodendritic local circuits. J Neurosci 27:9951-9961.
83. Yamaguchi M, Mori K (2005) Critical period for sensory experiencedependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci USA 102:9697-9702.
84. Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92:3371-3375.
85. Zuo Y, Lin A, Chang P, Gan WB (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181-189.