Executive Functions of Postweaning Protein Malnutrition in Mice

Sato, Shoko; Nakagawasai, Osamu; Tan-No, Koichi; Niijima, Fukie; Suzuki, Tomoyuki; Tadano, Takeshi

doi:10.1248/bpb.34.1413

Cited by 3 publications

(5 citation statements)

References 48 publications

(56 reference statements)

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“…This data may reflect differences in the plasticity between the developing and mature mouse brain. It is also consistent with our previous report on the induction in mice of behavioral effects such as alterations in cognitive function 21) and reduced anxiety behavior 41) by PM during the prepubertal but not postpubertal stage. Recently it has become apparent that brain development continues through adolescence and that prepubescence represents a period sensitive to nutritional deficits, 42) drug abuse 43) and isolation rearing.…”

Section: Discussionsupporting

confidence: 93%

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Enhanced Behavioral Response to Serotonin-Related Agonists in Postweaning Protein Malnourished Mice

Sato

Nakagawasai

Hayashi

et al. 2012

Biological & Pharmaceutical Bulletin

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We investigated whether postweaning protein malnutrition (PM) affects serotonergic systems. Mice were fed a PM diet or normal protein (control) diet from weaning (21 d of age). Twenty days later, we tested for behavioral effects of the selective serotonin (5-HT) 1A Key words protein malnutrition; serotonin 1A ; serotonin syndrome; head weaving; post-weaning period; mouse Serotonin (5-HT) is involved in the control of numerous physiological functions (e.g. food intake, thermoregulation, sleep patterns and nociception) 1) as well as in some psychiatric disorders such as anxiety and depression.2) These multiple actions are mediated through activation of at least 15 different families of serotonergic receptors.3) The 5-HT 1A receptor is one of the best described receptor subtypes and may be present on presynaptic as well as postsynaptic neurons.4) 5-HT 1A agonists have been successfully used in the treatment of anxiety disorders in human.5) However, excessive stimulation of postsynaptic 5-HT 1A receptor can lead to the 5-HT syndrome, a toxic condition displaying multiple clinical features. 6) In rodents, the administration of high doses of 5-HT 1A agonist, e.g. 8-hydroxy-N,N-dipropyl-2-aminotetralin (8-OH-DPAT), also elicits a 5-HT syndrome with typical major behavioral components such as flat body posture, hind limb abduction, forepaw treading, and head weaving. 7)5-HT concentrations are strongly influenced by undernourishment.8) 5-HT is synthesized from the amino acid precursor tryptophan and therefore is dependent on the latter's bioavailability. Brain levels of both are believed to increase as a result of metabolic adaptation to protein deficiency, which induces a decrease in the molar ratio of bound tryptophan to albumin. 9)However, some studies have reported either a decrease or no changes in brain serotonin levels following protein malnutrition (PM).10-12) Several experimental studies have focused on the consequences of prenatal (i.e., gestation period) and early postnatal (i.e., lactation period) malnutrition. PM during these developmental stages causes various atypical behaviors in rats, such as reduced anxiety, 13) decreased social interaction, 14) increased depressive behavior, 15) prepulse inhibition deficit 16) and impairment of memory-related behavior. 17) Moreover, a reduction in 5-HT 1A receptor levels and 5-HT uptake sites was reported in the hippocampus of prenatal PM rats.12) Since the 5-HT 1A receptor is considered to be a key receptor via which 5-HT participates in hippocampal dependent learning and memory functions, 18) PM may impact on cognitive performances as well. Thus, it is considered that the developmental period extending from gestation to weaning is critical with regards to PM. However, it has become apparent that brain development continues through adolescence.19) The age range for which the brain is vulnerable to the effects of malnutrition is potentially much greater than previously suspected but the threshold for malnutrition necessary to produce the behavioral alterations is unk...

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Section: Discussionsupporting

confidence: 93%

“…41) There are indications that hippocampal 5-HT 1A receptors are crucial for the modulation of these behaviors. 57,58) Indeed, it has been demonstrated that hippocampal 5-HT 1A receptor activation produces anxiolytic-like effects.…”

Section: Discussionmentioning

confidence: 99%

Enhanced Behavioral Response to Serotonin-Related Agonists in Postweaning Protein Malnourished Mice

Sato

Nakagawasai

Hayashi

et al. 2012

Biological & Pharmaceutical Bulletin

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“…One possible underlying mechanism of the negative relationship of underweight and overweight/obesity to academic performance is associated with worsened executive function 7,8,[14][15][16] , which is closely related to academic performance 12,25 . However, we could not elucidate the underlying mechanisms of the negative relationship of childhood underweight and overweight/obesity to the academic performance from the current findings.…”

Section: Discussionmentioning

confidence: 99%

“…Kar et al 14 showed that children with malnutrition demonstrated poor cognitive task performance requiring executive function. In an animal study, malnutrition intervention reduced brain weight associated with poor executive function in mice 16 . Although the mechanisms may be different, both overweight/obesity and underweight could impair executive function and, in turn, cause poor academic performance.…”

Section: Introductionmentioning

confidence: 97%

Longitudinal relationship of favorable weight change to academic performance in children

et al. 2020

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Although there is a growing consensus about the positive relationship between prevention of overweight/obesity and academic performance in children, relevant studies targeting the relationship between underweight and academic performance are scarce. This study aimed to examine the longitudinal relationship of favorable weight change to academic performance in schoolchildren. We analyzed 2-year longitudinal data derived from 197 seventh-grade children aged 12-13 years. Academic performance was assessed using the total grade points of five academic subjects. Body mass index (BMI) was calculated as body weight (kg)/height (m 2). A significant interaction effect of baseline BMI and BMI changes over 2 years (B = −0.10, SE B = 0.03, β = −0.40, t =-3.37, p < 0.001) was noted after controlling for confounders such as socioeconomic status, afterschool learning duration, screen time, exercise habits, and cardiorespiratory fitness. When the centered baseline BMI was outside the interval [−2.49, 3.21], the slope of the change in BMI was significant (p < 0.05). Simple slope analyses revealed a positive relationship of weight gain when baseline BMI = mean − 1 SD (B = 0.40, SE B = 0.18, β = 0.31, t = 2.20, p = 0.03) and weight loss when baseline BMI = mean + 1 SD (B = −0.26, SE B = 0.13, β = −0.20, t = −1.97, p = 0.05) to total grade points of five school subjects. A split-group validation was performed and robust results of original analyses were detected (i.e., significant interaction effect of baseline BMI and BMI changes over 2 years (group A: B = −0.11, SE B = 0.05, β = −0.47, t = −2.39, p = 0.02; group B: B = −0.14, SE B = 0.05, β = −0.47, t = −2.78, p = 0.007). Favorable changes in weight status, i.e., weight loss in children with overweight/obesity and weight gain in children with mild underweight/underweight, have a positive influence on academic performance in children independent of socioeconomic factors, learning habits, screen time, exercise habits, and cardiorespiratory fitness.

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“…Overall, the additive effect of hypoxia and rotation on body weight may be explained by 1) a decreased nutritional output to the pups due to rotation, 2) stress induced by changes in feeding behavior and/or metabolism and 3) changes in maternal care due to stressful effects of rotation on the mother, none of which are mutually exclusive and may all contribute partially or completely to decreased pup body weight. Certainly, handling, removing dams from pups (albeit typically for extended periods of time), changes in nutrition and maternal care, have all been shown to individually and collectively influence pup growth and brain development [4, 6, 8, 11, 15, 28, 32, 36, 42]. However, the relative contribution of these factors to changes observed in body and brain weight remains to be determined.…”

Section: Discussionmentioning

confidence: 99%

Contribution of maternal oxygenic state to the effects of chronic postnatal hypoxia on mouse body and brain development

Salmaso

Dominguez

Kravitz

et al. 2015

Neuroscience Letters

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1–2% of live births are to very low birth weight, premature infants that often show a developmental trajectory plagued with neurological sequelae including ventriculomegaly and significant decreases in cortical volume. We are able to recapitulate these sequelae using a mouse model of hypoxia where early postnatal pups are exposed to chronic hypoxia for one week. However, because the timing of hypoxic exposure is so early in development, dams and pups are housed together in the hypoxic chamber, and therefore dams are also subjected to the same hypoxic conditions as the pups. To understand the relative contribution of hypoxia directly on the pups as opposed to the indirect contribution mediated by the effects of hypoxia and potential alterations in the dam’s care of the pups, we examined whether reducing the dams exposure to hypoxia may significantly increase pup outcomes on measures that we have found consistently changed immediately following chronic hypoxia exposure. To achieve this, we rotated dams between normoxic and hypoxic conditions, leaving the litters untouched in their respective conditions and compared gross anatomical measures of normoxic and hypoxic pups with non-rotating or rotating mothers. As we expected, hypoxic-rearing decreased pup body weight, brain weight and cortical volume. Reducing the dam’s exposure to hypoxic conditions actually amplified the effects of hypoxia on body weight, such that hypoxic pups with rotating mothers showed significantly less growth. Interestingly, rotation of hypoxic mothers did not have the same deleterious effect on brain weight, suggesting the presence of compensatory mechanisms conserving brain weight and development even under extremely low body weight conditions. The factors that potentially contribute to these compensatory changes remain to be determined, however, nutrition, pup feeding/metabolism, or changes in maternal care are important candidates, acting either together or independently to change pup body and brain development.

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Executive Functions of Postweaning Protein Malnutrition in Mice

Cited by 3 publications

References 48 publications

Enhanced Behavioral Response to Serotonin-Related Agonists in Postweaning Protein Malnourished Mice

Enhanced Behavioral Response to Serotonin-Related Agonists in Postweaning Protein Malnourished Mice

Longitudinal relationship of favorable weight change to academic performance in children

Contribution of maternal oxygenic state to the effects of chronic postnatal hypoxia on mouse body and brain development

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