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. 2013 May 1;8(5):e62701.
doi: 10.1371/journal.pone.0062701. Print 2013.

Bi-parental care contributes to sexually dimorphic neural cell genesis in the adult mammalian brain

Gloria K Mak  1 , Michael C Antle, Richard H Dyck, Samuel Weiss
Affiliations

Bi-parental care contributes to sexually dimorphic neural cell genesis in the adult mammalian brain

Gloria K Mak et al. PLoS One. .

Abstract

Early life events can modulate brain development to produce persistent physiological and behavioural phenotypes that are transmissible across generations. However, whether neural precursor cells are altered by early life events, to produce persistent and transmissible behavioural changes, is unknown. Here, we show that bi-parental care, in early life, increases neural cell genesis in the adult rodent brain in a sexually dimorphic manner. Bi-parentally raised male mice display enhanced adult dentate gyrus neurogenesis, which improves hippocampal neurogenesis-dependent learning and memory. Female mice display enhanced adult white matter oligodendrocyte production, which increases proficiency in bilateral motor coordination and preference for social investigation. Surprisingly, single parent-raised male and female offspring, whose fathers and mothers received bi-parental care, respectively, display a similar enhancement in adult neural cell genesis and phenotypic behaviour. Therefore, neural plasticity and behavioural effects due to bi-parental care persist throughout life and are transmitted to the next generation.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Bi-parentally raised males display enhanced neurogenesis, which is transmitted to the next generation of male offspring.
(A) Offspring raised in maternal-only (MO), maternal-virgin (MV) and maternal-paternal (MP) conditions display sexually dimorphic enhancement of adult dentate gyrus (DG) cell proliferation (mean±SEM), where MV and MP males have more BrdU-labeled cells in the DG compared to MO males (n = 5 per group). (B) Cell proliferation in the SVZ is no different among adult male and female offspring raised in different parental conditions (mean±SEM). (C and D) Representative fluorescent micrographs of BrdU-NeuN double labeled cells in the DG of males raised in a single parent environment and bi-parental (MV) environment, respectively. Bars represent 50 µm. (E) MV and MP males show enhanced neurogenesis in the DG (mean±SEM) (n = 5 per group). (F) Males raised in a maternal-only (MO) environment, but sired by MV or MP fathers have more BrdU-labeled cells (mean±SEM) versus MO males sired by MO fathers (n = 5 per group). (G) Males raised in a MO environment, but sired by MV or MP fathers have more BrdU-NeuN double-labeled cells in the DG (mean±SEM) (n = 4 per group).
Figure 2
Figure 2. Males with enhanced dentate gyrus neurogenesis display increased freezing during contextual fear conditioning.
(A) MO, MV, and MP males show no difference in cue fear conditioning (mean±SEM). (B) MV and MP males display enhanced freezing in contextual fear conditioning, compared to MO males (mean±SEM) (n = 12 per group). (C and D) MO, MV, and MP females, which display no difference in dentate gyrus neurogenesis, show no difference in cue fear conditioning (mean±SEM) or contextual fear conditioning (mean±SEM), respectively. (E) MO males sired by MO, MV, or MP fathers display no difference in cue fear conditioning (mean±SEM). (F) However, MO males sired by MV or MP fathers display a greater percentage of freezing in contextual fear conditioning (mean±SEM) (MO males (P: MO male×MO female) (n = 10), MO males (P: MV male×MO female) (n = 7), and MO males (MP male×MO female) (n = 9)).
Figure 3
Figure 3. Females raised in a bi-parental environment have more newly generated myelinating oligodendrocytes and myelinated axons in the corpus callosum, which is transmitted to the next generation of female offspring.
(A) Offspring raised in maternal-only (MO), maternal-virgin (MV) and maternal-paternal (MP) conditions, display sexually dimorphic enhancement of adult corpus callosum (CC) cell proliferation. Fluorescent micrograph of BrdU-labeled cells in the CC. Bar represents 50 µm. (B) MV and MP females have increased numbers of BrdU-labeled cells in the CC compared to MO females (mean±SEM) (n = 4 per group). (C) Fluorescent micrograph of PDGFRa-BrdU double-labeled cells in the CC. Bar represents 50 µm. (D) MV and MP females display more PDGFRa-BrdU double-labeled cells in the CC than MO females (mean±SEM) (n = 4 per group). (E) Fluorescent micrograph of GSTπ-BrdU double-labeled cells in the CC. Bar represents 50 µm. (F) MV and MP females display enhanced oligodendrogliogenesis in the CC compared to MO females (mean±SEM) (n = 4 per group). (G) Electron micrograph of axons in the genu of CC. (H) There are more myelinated axons in the genu of CC in MV and MP females than MO females (mean±SEM) (n = 42 (MO images), n = 56 (MV images) and n = 56 (MP images)). (I) Females raised in a MO environment, but sired by MV or MP mothers have more BrdU-labeled cells (mean±SEM) (MO females (n = 4 per group). (J) Females raised in a MO environment, but sired by MV or MP mothers have more BrdU-GSTπ double-labeled cells in the corpus callosum (mean±SEM) (n = 4 per group).
Figure 4
Figure 4. Females with enhanced numbers of newly generated myelinating oligodendrocytes and myelinated axons in the corpus callosum display greater bilateral motor coordination and preference for social investigation.
(A) MV and MP females display less slipping on the horizontal ladder rung task than MO females (n = 11 per group). (B) MV and MP females also show a greater preference for social investigation as they spend more time investigating a novel conspecific than an inanimate object (mean±SEM) (n = 10 per group). (C and D) MO, MV, and MP males, which do not display enhanced oligodendrogliogenesis, show no difference in performance on the horizontal ladder rung. MO, MV, and MP males all demonstrate a greater preference for investigating the novel conspecific versus the inanimate object (mean±SEM) (n = 8 per group). (E) MO females sired by MV or MP mothers demonstrate less slipping on the horizontal ladder rung over time (mean±SEM) (n = 10 per group). (F) MO females sired by MV or MP mothers display greater investigation towards a novel conspecific (mean±SEM) (MO females (P: MO female×MO male) (n = 10), MO females (MV female×MO male) (n = 11) and MO females (MP female×MO male) (n = 13)).
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