Experience‐dependent transcriptional regulation in juvenile brain development

Sakai, Akiko; Sugiyama, Sayaka

doi:10.1111/dgd.12571

Cited by 9 publications

(5 citation statements)

References 96 publications

(152 reference statements)

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“…Pellis et al (2023) noted that juvenile play behavior in rats promotes increased behavioral skill and social competency during adulthood, and suggested that a general benefit of play may be to refine or improve skills and behaviors that can be applied adaptively across a variety of social and nonsocial contexts. Various aspects of brain development exhibit plasticity during neonatal and juvenile periods, and a range of experiences after birth can direct elements of neural and behavioral development (Johnson, 2001;Stiles and Jernigan, 2010;Kolb and Gibb, 2011;Sakai and Sugiyama, 2018). Various brain regions help to modulate the expression of play behavior in mammals (Pellis and Iwaniuk, 2004;Siviy, 2016;Achterberg and Vanderschuren, 2023).…”

Section: Discussionmentioning

confidence: 99%

Disruption of social play influences development of caution in juvenile ground squirrels

Ryan,

Kuan,

Nunes

2024

Front. Ethol.

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Play behavior is common in a range of mammalian species and can have important influences on early development. We evaluated possible influences of social play on the development of behavior along the caution/boldness continuum in juvenile Belding’s ground squirrels (Urocitellus beldingi). We disrupted juvenile squirrels engaged in play by walking toward them until their play interactions stopped. We used undisrupted juveniles and juveniles disrupted while not engaged in play as controls. Caution was measured with behavioral tests during which a human intruder walked toward a squirrel and recorded the distances at which the squirrel first noticed and then fled from the intruder. Rates of social play were lower and play bouts were shorter in play-disrupted juveniles than in undisrupted and nonplay-disrupted juveniles. The distances at which juveniles noticed and fled from an intruder increased across the developmental period in which play primarily occurs, suggesting increases in caution across this interval. Increases in the distances to notice and flee from an intruder did not differ between undisrupted and nonplay-disrupted juveniles, but were greater in these groups than in play-disrupted juveniles. These results are consistent with social play behavior contributing to the development of cautious responses in juvenile U. beldingi.

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Section: Discussionmentioning

confidence: 99%

Disruption of social play influences development of caution in juvenile ground squirrels

Ryan,

Kuan,

Nunes

2024

Front. Ethol.

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“…Various brain regions help to modulate the expression of play behavior in mammals (Pellis and Iwaniuk 2004;Siviy 2016;Vanderschuren et al 2016). Moreover, experiences after birth can play an important role in directing specific aspects of neural and behavioral development in mammals (Johnson 2001;Stiles and Jernigan 2010;Sakai and Sugiyama 2018). Pellis et al (2010Pellis et al ( , 2014 suggested that social play behavior refines the control that the prefrontal cortex has over other brain regions, facilitating more nuanced neural responses and more adaptable behavior later in life.…”

Section: Discussionmentioning

confidence: 99%

Social play predicts caution in juvenile Belding’s ground squirrels (Urocitellus beldingi)

Shehan,

Hernandez,

Rodriguez

et al. 2023

Journal of Mammalogy

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Play is an important component of development in a range of mammalian species, and may provide adaptive benefits for young individuals in some cases. We evaluated the hypothesis that social play in juvenile Belding’s ground squirrels (Urocitellus beldingi) promotes development of cautious responses when individuals are confronted with a potential threat. We observed the play behavior of juvenile U. beldingi across the developmental period in which play primarily occurs. To measure caution, we conducted behavioral tests on individual squirrels at the beginning and toward the end of the play period, and again when the individuals were yearlings. During tests we recorded the distances at which squirrels first noticed and fled from a human intruder. In initial tests, juveniles with yearling mothers responded to intruders at greater distances than did juveniles with older mothers suggesting maternal effects on the development of caution. Distances at which juveniles noticed and fled from an intruder increased across the play interval, suggesting increased caution to a potential threat as early development progresses. Social play was a reliable predictor of increases in caution, with juveniles who engaged in social play at higher rates having greater increases in the distance to notice and flee from an intruder. Distances to flee from an intruder at the end of the play interval were reliable predictors of distances to flee from an intruder as a yearling, suggesting consistency in cautious responses among individual U. beldingi over time. Rates of social play as a juvenile were reliable predictors of distances to notice and flee from an intruder as a yearling, suggesting that possible influences of play behavior on cautious responses extend beyond the juvenile period.

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“…17 A related issue is that perturbing OTX2 in the adult VTA may not be effective because OTX2 activity may only be required during a specific developmental window 17 or critical period, which is consistent with a known role for OTX2 in critical period plasticity in the visual system. 37,38 Finally, it is possible that OTX2 in the VTA just doesn't play a role in ethanol intake. Otx2 is expressed in select regions of the CNS and could presumably be involved in binge-like ethanol drinking through its transcriptional activity in those regions.…”

Section: Discussionmentioning

confidence: 99%

Binge-Like Ethanol Drinking Increases Otx2, Wnt1, and Mdk Gene Expression in the Ventral Tegmental Area of Adult Mice

Coles

Lasek

2021

J Exp Neurosci

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Alcohol use disorder is associated with pathophysiological changes in the dopaminergic system. Orthodenticle homeobox 2 (OTX2) is a transcription factor important for the development of dopaminergic neurons residing in the ventral tegmental area (VTA), a critical region of the brain involved in drug reinforcement. Previous studies have demonstrated that ethanol exposure during embryonic development reduces Otx2 mRNA levels in the central nervous system. We hypothesized that levels of OTX2 would be altered by binge-like ethanol consumption in adult animals. To test this, Otx2 mRNA and protein levels in the mouse VTA were measured by quantitative real-time PCR and western blotting, respectively, after mice drank ethanol for 4 days in a procedure that elicits binge levels of ethanol consumption (drinking in the dark). Expression of known and putative OTX2 transcriptional target genes ( Sema3c, Wnt1, and Mdk) were also measured in the VTA after ethanol drinking. Otx2 mRNA and protein levels were elevated in the VTA 24 hours after the fourth drinking session and there was a corresponding increase in the expression of Mdk transcript. Interestingly, Wnt1 transcript was elevated in the VTA immediately after the fourth drinking session but returned to control levels 24 hours later. We next investigated if viral-mediated reduction of Otx2 in the mouse VTA would alter ethanol or sucrose intake. Lentiviral vectors expressing a shRNA targeting Otx2 or a control shRNA were injected into the VTA and mice were tested in the drinking in the dark protocol for ethanol and sucrose drinking. Reducing levels of OTX2 in the VTA did not alter ethanol or sucrose consumption. One limitation is that the extent of OTX2 reduction may not have been sufficient. Although OTX2 in the VTA may not play a role in binge-like drinking in adult mice, OTX2 could contribute to ethanol-induced transcriptional changes in this region.

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Experience‐dependent transcriptional regulation in juvenile brain development

Cited by 9 publications

References 96 publications

Disruption of social play influences development of caution in juvenile ground squirrels

Disruption of social play influences development of caution in juvenile ground squirrels

Social play predicts caution in juvenile Belding’s ground squirrels (Urocitellus beldingi)

Binge-Like Ethanol Drinking Increases Otx2, Wnt1, and Mdk Gene Expression in the Ventral Tegmental Area of Adult Mice

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