Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: Interaction with a brief, daily maternal separation

Cannizzaro, Carla; Plescia, Fulvio; Martire, Maria; Gagliano, M.; G, Cannizzaro; Mantia, Giacoma; Cannizzaro, Emanuele

doi:10.1016/j.bbr.2005.12.010

Cited by 72 publications

(56 citation statements)

References 67 publications

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“…Early handling made the rats in this group less fearful, less stressed, and more risk-takers in the light-dark test, as evidenced by more ambulatory behavior in the light area of this arena. This finding corroborates other published studies in which a 15-minute separation period results in attenuated anxiety-like behavior and increased risk-taking in an open-field (Cannizzaro et al, 2006, Madruga et al, 2006 as well as reductions in conditioned fear responding (Meerlo et al, 1999). MS had the exact opposite effect, as seen in the light-dark test on P29, which differentiated between the three groups more than any other behavior measure in any other session of this study (P28, P29, P30).…”

Section: Discussionsupporting

confidence: 81%

Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats

Spivey

Barrett

Padilla

et al. 2008

Behavioural Processes

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This is the first study of the effects of mother-infant separation (MS) on adolescent behavior of Holtzman rats. Different rat strains, such as Harlan Sprague-Dawley and Holtzman, share a common origin. However, MS may lead to hypoactive behavioral effects in Holtzman rats because of their greater susceptibility to show depressive-like responses to stress. Sixty Holtzman pups were divided into 3 groups at postnatal day 2 (P2). For 10 days, the MS group was separated 6 hours daily and the early handled (EH) group 15 min daily. A standard facility reared (SFR) group was not separated. Animals were tested for novel open-field activity (P28), defensive withdrawal in a light-dark (LD) apparatus (P29) and familiar open-field (P30). Behavioral measures were classified into general activity (ambulatory and short movement time), orienting (rearing time) and risk-taking (velocity and exposed zone time). MS rats displayed reductions in general activity and risk-taking, and increases in orienting time. In contrast, EH favored risk-taking behavior, which may be consistent with previous findings implicating early handling as beneficial in coping with stress. Sex differences in these behaviors were limited. This study suggests a genetic predisposition in Holtzman rats for predominantly hypoactive/anxiety-like behaviors when exposed to an early life stressor.

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Section: Discussionsupporting

confidence: 81%

Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats

Spivey

Barrett

Padilla

et al. 2008

Behavioural Processes

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“…We chose not to employ close-monitoring techniques, including blood sampling for measurement of plasma corticosterone, because such procedures would add stress to the dams and unborn fetus. Restraining the dams only once during late pregnancy and tail pricking for a blood sample have been shown to elevate corticosterone concentration in the offspring (6). However, we recorded the body weight of the dams 1 day before delivery and 1 day after delivery in subsequent experiments and found no evidence that they were avoiding or were stressed by the HV diet.…”

Section: Discussionmentioning

confidence: 90%

High multivitamin intake by Wistar rats during pregnancy results in increased food intake and components of the metabolic syndrome in male offspring

Szeto¹,

Aziz²,

Das³

et al. 2008

American Journal of Physiology-Regulatory, Integrative and Comp

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The effect of high multivitamin intake during pregnancy on the metabolic phenotype of rat offspring was investigated. Pregnant Wistar rats (n=10 per group) were fed the AIN-93G diet with the recommended vitamin (RV) content or a 10-fold increase [high vitamin (HV) content]. In experiment 1, male and female offspring were followed for 12 wk after weaning; in experiment 2, only males were followed for 28 wk. Body weight (BW) was measured weekly. Every 4 wk, after an overnight fast, food intake over 1 h was measured 30 min after a gavage of glucose or water. An oral glucose tolerance test was performed every 3-5 wk. Postweaning fasting glucose, insulin, ghrelin, glucagon-like peptide-1, and systolic blood pressure were measured. No difference in BW at birth or litter size was observed. Food intake was greater in males born to HV dams (P<0.05), and at 28 wk after weaning, BW was 8% higher (P<0.05) and fat pad mass was 27% higher (P<0.05). Food intake reduction after the glucose preload was nearly twofold less in males born to HV dams at 12 wk after weaning (P<0.05). Fasting glucose, insulin, and ghrelin were 11%, 62%, and 41% higher in males from HV dams at 14 wk after weaning (P<0.05). Blood glucose response was 46% higher at 23 wk after weaning (P<0.01), and systolic blood pressure was 16% higher at 28 wk after weaning (P<0.05). In conclusion, high multivitamin intake during pregnancy programmed the male offspring for the development of the components of metabolic syndrome in adulthood, possibly by its effects on central mechanisms of food intake control.

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“…For instance, prolonged daily maternal separation has been shown to either impair (Huot et al, 2002;Uysal et al, 2005) or enhance (Pryce et al, 2003) later spatial learning and memory. The effects of brief separation are less pronounced (Gibb and Kolb, 2005;Cannizzaro et al, 2006). Furthermore, whereas acquisition of fear conditioning for context and tone is not affected by either brief or prolonged maternal separation (Pryce et al, 2003;Kosten et al, 2005Kosten et al, , 2006, adult retention of conditioned fear may be reduced following maternal separation (Meerlo et al, 1999;Kosten et al, 2005Kosten et al, , 2006.…”

Section: Introductionmentioning

confidence: 91%

Neonatal maternal separation alters adult eyeblink conditioning and glucocorticoid receptor expression in the interpositus nucleus of the cerebellum

Wilber

Southwood

Sokoloff

et al. 2007

Developmental Neurobiology

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Neonatal maternal separation alters learning and memory. Glucocorticoids also modulate adult learning and memory, and neonatal maternal separation alters forebrain glucocorticoid receptor (GR) concentrations. We used eyeblink classical conditioning to assess the effect of neonatal maternal separation on associative learning. We assessed delay eyeblink conditioning, GR expression, and total neuron number in the interpositus nucleus, a critical site of plasticity in eyeblink conditioning, in adult rats that had undergone either standard animal facilities rearing, handling for 15 min, or maternal separation for either 15 or 60 min per day on postnatal days 2-14. At 2-3 months of age, delay eyeblink classical conditioning was assessed. Brains were processed for GR immunohistochemistry, and GR expression in the interpositus nucleus was assessed using a computer-based densitometry system. Neuron counts and nuclear volumes were obtained from an alternate series of thionin-stained sections. Maternal separation significantly impaired eyeblink conditioning in male but not female rats. Handling and maternal separation did not significantly affect interpositus neuron number and volume. However, prolonged maternal separation significantly increased GR expression in the posterior interpositus in males, and increases were correlated with eyeblink conditioning. In female rats, maternal separation and handling did not significantly alter interpositus neuron number, volume, or GR protein expression, and GR expression did not correlate with eyeblink conditioning. Thus, neonatal maternal separation produces adult deficits in eyeblink conditioning and alterations in GR expression in its neural substrate in a sex-dependent manner.

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Single, intense prenatal stress decreases emotionality and enhances learning performance in the adolescent rat offspring: Interaction with a brief, daily maternal separation

Cited by 72 publications

References 67 publications

Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats

Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats

High multivitamin intake by Wistar rats during pregnancy results in increased food intake and components of the metabolic syndrome in male offspring

Neonatal maternal separation alters adult eyeblink conditioning and glucocorticoid receptor expression in the interpositus nucleus of the cerebellum

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