Maternal chewing during prenatal stress ameliorates stress-induced hypomyelination, synaptic alterations, and learning impairment in mouse offspring.
Maternal chewing during prenatal stress attenuates both the development of stress-induced learning deficits and decreased cell proliferation in mouse hippocampal dentate gyrus. Hippocampal myelination affects spatial memory and the synaptic structure is a key mediator of neuronal communication. We investigated whether maternal chewing during prenatal stress ameliorates stress-induced alterations of hippocampal myelin and synapses, and impaired development of spatial memory in adult offspring. Pregnant mice were divided into control, stress, and stress/chewing groups. Stress was induced by placing mice in a ventilated restraint tube, and was initiated on day 12 of pregnancy and continued until delivery. Mice in the stress/chewing group were given a wooden stick to chew during restraint. In 1-month-old pups, spatial memory was assessed in the Morris water maze, and hippocampal oligodendrocytes and synapses in CA1 were assayed by immunohistochemistry and electron microscopy. Prenatal stress led to impaired learning ability, and decreased immunoreactivity of myelin basic protein (MBP) and 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNPase) in the hippocampal CA1 in adult offspring. Numerous myelin sheath abnormalities were observed. The G-ratio [axonal diameter to axonal fiber diameter (axon plus myelin sheath)] was increased and postsynaptic density length was decreased in the hippocampal CA1 region. Maternal chewing during stress attenuated the prenatal stress-induced impairment of spatial memory, and the decreased MBP and CNPase immunoreactivity, increased G-ratios, and decreased postsynaptic-density length in the hippocampal CA1 region. These findings suggest that chewing during prenatal stress in dams could be an effective coping strategy to prevent hippocampal behavioral and morphologic impairments in their offspring.
Department of Pediatric Dentistry, Asahi University School of Dentistry, 1851 Hozumi, Mizuho, Gifu 501-0296, Japan.
Ayumi
A
Suzuki
Department of Pediatric Dentistry, Asahi University School of Dentistry, 1851 Hozumi, Mizuho, Gifu 501-0296, Japan.
Mitsuo
M
Iinuma
Department of Pediatric Dentistry, Asahi University School of Dentistry, 1851 Hozumi, Mizuho, Gifu 501-0296, Japan.
Sakurako
S
Hayashi
Department of Molecular Diagnostics, Kitasato University School of Allied Health Science, Kitasato 1-15-1, Minamiku, Sagamihara, Kanagawa 252-0373, Japan.
Yuichi
Y
Sato
Department of Anatomy, School of Medicine, University of Occupational and Environmental Health, 1-1 Iseigaoka, Yahatanishi-ku, Kitakyushu, Fukuoka 807-8555, Japan.
Kagaku
K
Azuma
Seijoh University Graduate School of Health Care Studies, 2-172, Fukinodai, Tokai, Aichi 476-8588, Japan. Electronic address: kubo@seijoh-u.ac.jp.
Kin-Ya
KY
Kubo
D000818:Animals; D004195:Disease Models, Animal; D005260:Female; D006624:Hippocampus / Q000254:growth & development* / Q000378:metabolism / Q000473:pathology; D007859:Learning Disabilities / Q000209:etiology / Q000378:metabolism / Q000473:pathology / Q000517:prevention & control*; D008297:Male; D008409:Mastication; D018782:Maze Learning; D051379:Mice; D009186:Myelin Sheath / Q000378:metabolism / Q000473:pathology; D009836:Oligodendroglia / Q000378:metabolism / Q000473:pathology; D011247:Pregnancy; D011297:Prenatal Exposure Delayed Effects / Q000517:prevention & control*; D011897:Random Allocation; D012149:Restraint, Physical; D065852:Spatial Memory; D013315:Stress, Psychological / Q000628:therapy*; D013569:Synapses / Q000378:metabolism / Q000473:pathology; D014934:Wood
Chewing; Hippocampus; Myelin sheath; Prenatal stress; Synapse