A critical period for social experience-dependent oligodendrocyte maturation and myelination
Open accessAbstract
A Critical Period for Glia: The brain develops in fits and starts—while one system is completed, another system may still be under construction. Such transient states are known as critical periods, and during these specific aspects of brain development may become more sensitive to outside agents than they would be later. Makinodan et al. (p. 1357 ) observed the effect of environmental conditions on the brains of mice bioengineered to develop fluorescent oligodendrocytes. The mice were exposed to a variety of social conditions during rearing, ranging from isolation to a normal laboratory cage setting, or to settings enriched with extra buddies and a steady rotation of new play toys. The results show that social isolation leaves a developmental trace that persists into adulthood. Specifically, they found that oligodendrocytes, which produce the myelin that insulates neurons, were underdeveloped, suggesting that there may be a critical period that governs development of these glial oligodendrocyte cells.
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Social isolation impairs adult myelination in the mouse prefrontal cortex and causes behavioral deficits.
“Social isolation impairs adult myelination in the mouse prefrontal cortex and causes behavioral deficits (Liu et al., 2012 ; Makinodan et al., 2012 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as Makinodan et al., 2012
The paper reports that isolation immediately after weaning (P21–P35) alters mouse prefrontal-cortex myelination and produces behavioral deficits that persist into adulthood. The claim omits that critical-period restriction: the paper reports that isolation begun after P35 did not produce those effects. (LLM, conf=0.86)
Experimental — accuracy not yet measuredImpaired regulation of myelination or impairment of myelin itself frequently accompanies learning deficits, cognitive dysfunction, and aging.
“Impaired regulation of myelination or impairment of myelin itself frequently accompanies learning deficits, cognitive dysfunction, and aging (Bennett & Madden, 2014 ; Liu et al., 2012 ; Makinodan, Rosen, Ito, & Corfas, 2012 ;McKenzie et al., 2014 ; Xiao et al., 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as Makinodan, Rosen, Ito, & Corfas, 2012
The paper’s main text reports that juvenile social isolation in mice altered prefrontal myelination and working memory, supporting the link to cognitive dysfunction. It does not establish that myelin impairment frequently accompanies learning deficits or aging; its findings concern a specific juvenile-isolation condition, not aging generally. (LLM, conf=0.87)
Experimental — accuracy not yet measuredSocial conditions experienced by mice can influence the morphological complexity of their OLs (including the number of internodes per OL) and this is mediated by Neuregulin signaling through ErbB3 receptors on OLs.
“Recently, it has been shown that the social conditions experienced by mice can influence the morphological complexity of their OLs (including the number of internodes per OL) and that this is mediated by Neuregulin signaling through ErbB3 receptors on OLs (Makinodan et al., 2012).”
From Oligodendrocyte Dynamics in the Healthy Adult CNS: Evidence for Myelin Remodeling (2013) · cites this paper as Makinodan et al., 2012
The paper reports that juvenile social isolation produced simpler oligodendrocytes with fewer internodes in the mouse medial prefrontal cortex (main text, Fig. 1; page unavailable). It links these effects to neuregulin-1/ErbB3 signaling, but says that pathway accounts for them 'at least in part' and does not rule out other mechanisms. The claim omits that qualification and the regional and developmental limits of the findings. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe DFC is a brain region of late myelination which performs a critical role in the organization of behavioral, linguistic, and cognitive functions.
“The present results clearly show a profound deficit in white matter maturation in individuals with DS during infancy and adolescence in DFC, a brain region of late myelination which performs a critical role in the organization of behavioral, linguistic, and cognitive functions (Fuster, 2002; Makinodan et al., 2012).”
From Down Syndrome Developmental Brain Transcriptome Reveals Defective Oligodendrocyte Differentiation and Myelination (2016) · cites this paper as Makinodan et al., 2012
In the paper’s main text (page not provided), Makinodan et al. report a critical period of myelination in the mouse medial prefrontal cortex and link its maturation to social behavior and working memory. That supports a role in behavioral and cognitive function, but the paper does not establish that the DFC is a late-myelinating region or address linguistic functions. (LLM, conf=0.86)
Experimental — accuracy not yet measuredEarly environmental deprivation in animals also causes poor white matter integrity from reduced myelination and axon-sprouting, particularly in posterior corpus callosum and prefrontal cortex.
“poor white matter integrity resulting from reduced myelination and axon-sprouting also occurs in animals exposed to early environmental deprivation, particularly in the posterior corpus callosum(82) and prefrontal cortex (PFC).(83)”
From Neglect as a violation of species-expectant experience: neurodevelopmental consequences (2017) · cites this paper as [83]
In rodents, depending on the duration of juvenile social isolation, increased or decreased sociability in adulthood has been reported, suggesting that adolescence is a sensitive period for establishing social behavior later in life.
“In rodents, depending on the duration of juvenile social isolation, increased or decreased sociability in adulthood has been reported, suggesting that adolescence is a sensitive period for establishing social behavior later in life (Yamamuro et al., 2020; Yamamuro et al., 2018; Makinodan et al., 2012; Rivera-Irizarry et al., 2020).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Makinodan et al., 2012
In male mice, juvenile social isolation for two weeks immediately after weaning (p21-35) reduces sociability in adulthood compared with group-housed mice.
“Juvenile social isolation reduces sociability in adulthood, but the neural circuit mechanisms are poorly understood.”
From A prefrontal–paraventricular thalamus circuit requires juvenile social experience to regulate adult sociability in mice (2020) · cites this paper as [5]
Social isolation from P20-40 in mice disrupts medial PFC function and myelination, but later isolation from P40-60 does not.
“Social isolation from P20–40 in mice disrupts medial PFC function and myelination, but later isolation from P40–60 does not (Makinodan et al., 2012).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Makinodan et al., 2012
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“Social isolation impairs adult myelination in the mouse prefrontal cortex and causes behavioral deficits (Liu et al., 2012; Makinodan et al., 2012).”
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- Authors
- Makinodan, M., Rosen, K. M., Ito, S., & Corfas, G.
- Affiliations
- Boston Children's Hospital (US)
- Harvard University (US)
- Corresponding author
- Corfas, Gabriel
- Venue
- Science
- Published
- 2012-09-14
- Volume
- 337
- Issue
- 6100
- Pages
- 1357-1360
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4165613
- OpenAlex
- W1967937854
- Cited by
- 922
- References
- 38
- Citations by year
- 2026: 46 · 2025: 58 · 2024: 81 · 2023: 73 · 2022: 92 · 2021: 86 · 2020: 78 · 2019: 77 · 2018: 59 · 2017: 65 · 2016: 56 · 2015: 59 · 2014: 41 · 2013: 43 · 2012: 6
- FWCI
- 16.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01 NS35884, R01NS035884)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655, P30HD-18655)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- social isolation, social deprivation, oligodendrocyte maturation, myelination, white matter, prefrontal cortex, neuregulin-1, cognitive function, critical period, social experience
- MeSH terms
- Animals, Behavior, Animal, Female, Male, Mice, Inbred C57BL, Myelin Sheath, Oligodendroglia, Social Isolation, Signal Transduction, Prefrontal Cortex, Mice, Knockout, Neuregulin-1, Receptor, ErbB-3, Green Fluorescent Proteins, Mice
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