Strain of foster mother determines long-term effects of early handling: Evidence for maternal mediation

Hennessy, Michael B.; Vogt, Jerry L.; Levine, Seymour

doi:10.3758/bf03327019

Cited by 22 publications

(9 citation statements)

References 37 publications

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“…In recent studies, we have found evidence for the idea that the effects of handling on either endocrine (Liu et al 1997) or behavioral/emotional (Caldji et al 1998) responses to stress are mediated by handlinginduced changes in maternal behavior (Smotherman and Bell 1980;Hennessy et al 1982). Mothers of handled pups exhibit increased licking/grooming and arched-back nursing (Lee and Williams 1975;Liu et al 1997;Caldji et al 1998).…”

Section: Discussionmentioning

confidence: 99%

The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat

Caldji

Francis

Sharma

et al. 2000

Neuropsychopharmacology

516

333

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We compared the effects of handling or maternal separation from the day following birth until postnatal day 14 on behavioral responses to novelty and on GABA A and central benzodiazepine (CBZ) receptor levels in the rat. As adults, handled animals showed reduced startle responsivity, increased exploration in a novel open field, and decreased novelty-induced suppression of feeding relative to the handled (H) and/or maternal separation (MS) groups. As compared with handled animals, both nonhandled (NH) and MS animals displayed: (1) reduced GABA A receptor levels in the locus coeruleus (LC) and the n. tractus solitarius (NTS); (2) reduced CBZ receptor sites in the central and lateral n. of the amygdala, the frontal cortex, and in the LC and NTS; and (3) The development of behavioral and endocrine responses to acute stress is greatly influenced by the early postnatal rearing environment (for reviews see Levine 1975;Denenberg 1964;Meaney et al. 1996). These environmental effects persist throughout the life of the animal, resulting in stable individual differences in stress reactivity. Indeed, there is considerable plasticity in the development of these systems. Postnatal handling during the first week of life greatly decreases behavioral fearfulness and hypothalamic-pituitary-adrenal (HPA) responses to stress; whereas, repeated periods of prolonged maternal separation produce enhanced reactivity. Increased stress reactivity has been associated with an enhanced risk for several forms of illness, including affective disorders, diabetes, autoimmune disorders, and coronary heart disease (Chrousos and Gold 1992;Higley et al. 1991;McEwen and Steller 1993;Seckl and Meaney 1994). Thus, in determining the magnitude of behavioral and endocrine responses to stress, early life events NO . 3 contribute to vulnerability to disease in later life (Seckl and Meaney 1994). The critical question, then, concerns the mechanisms for these early environmental effects on the development of behavioral and endocrine responses to stress.Postnatal handling has been shown to decrease fearfulness to novelty (Levine 1962(Levine , 1957Denenberg 1964;Bodnoff et al. 1987). As adults, handled (H) rats show reduced novelty-induced suppression of appetitive behavior and increased exploration in novel environments. The behavioral effects of repeated maternal separation in rats are less documented, although, in primates, there is considerable evidence for enhanced fearfulness in animals exposed to maternal separation in early life (Sackett 1969).The mechanisms underlying these early environmental effects on behavioral responses to novelty are unclear. Bodnoff et al. (1987) reported that neonatal handling increased forebrain central benzodiazepine (CBZ) receptor levels, with no indication of where in the forebrain such differences might exist. Nevertheless, these data are certainly consistent with the wellestablished, anxiolytic effects of benzodiazepines on behavioral responses to novelty (see File 1995 for a review). Moreover, these findings are a...

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Section: Discussionmentioning

confidence: 99%

The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat

Caldji

Francis

Sharma

et al. 2000

Neuropsychopharmacology

516

333

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“…While these results are very preliminary (e.g., cortisol responses were not measured following a second separation; only one time point was assessed), they suggest that reduced glucocorticoid suppression of proinflammatory processes during subsequent separations may help account for the more-rapid febrile response and increased passive behavior. In rats and mice, lasting effects of early separation on glucocorticoid levels and other measures often appear to be mediated by the treatment of the pups by the mother upon return to the home cage [e.g.,30,38]. In the precocial guinea pig, by contrast, active maternal care rarely is observed beyond the first week postpartum [35], even following separation and reunion [25].…”

Section: Discussionmentioning

confidence: 99%

Sensitization of depressive-like behavior during repeated maternal separation is associated with more-rapid increase in core body temperature and reduced plasma cortisol levels

Yusko

Hawk

Schiml

et al. 2012

Physiology & Behavior

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Infant guinea pigs exhibit a 2-stage response to maternal separation: an initial active stage, characterized by vocalizing, and a second passive stage marked by depressive-like behavior (hunched posture, prolonged eye-closure, extensive piloerection) that appears to be mediated by proinflammatory activity. Recently we found that pups showed an enhanced (i.e., sensitized) depressive-like behavioral response during repeated separation. Further, core body temperature was higher during the beginning of a second separation compared to the first, suggesting a more-rapid stress-induced febrile response to separation the second day, though the possibility that temperature was already elevated prior to the second separation could not be ruled out. Therefore, the present study examined temperature prior to, and during, 2 daily separations. We also examined the temperature response to a third separation conducted 3 days after the second, and assessed the effect of repeated separation on plasma cortisol levels. Core temperature did not differ just prior to the separations, but showed a more-rapid increase and then decline during both a second and third separation than during a first. Temperature responses were not associated with changes in motor activity. Depressive-like behavior was greater during the second and third separations. Pups separated a first time showed a larger plasma cortisol response at the conclusion of separation than did animals of the same age separated a third time. In all, the results indicate that the sensitization of depressive-like behavior during repeated separations over several days is accompanied by a more-rapid febrile response that may be related to a reduction of glucocorticoid suppression.

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“…At present, the nature of these factors remains to be elucidated. An obvious but unlikely possibility is suggested by evidence indicating that the effects of early postnatal handling on behavioural and neuroendocrine responses to stress are mediated by changes in maternal behaviour (Smotherman & Bell, 1980; Hennessy et al ., 1982; Liu et al ., 1997; Caldji et al ., 1998). Indeed, mothers respond to H pups with increased licking/grooming behaviour and arched‐back nursing (Lee & Williams, 1975; Liu et al ., 1997; Caldji et al ., 1998).…”

Section: Discussionmentioning

confidence: 99%

Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats

Brake

Zhang

Diorio

et al. 2004

Eur J of Neuroscience

293

216

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While many experiment with drugs, relatively few individuals develop a true addiction. We hypothesized that, in rats, such individual differences in the actions of addictive drugs might be determined by postnatal rearing conditions. To test this idea, we investigated whether stimulant- and stress-induced activation of nucleus accumbens dopamine transmission and dopamine-dependent behaviours might differ among adults rats that had been either repeatedly subjected to prolonged maternal separation or a brief handling procedure or left undisturbed (non-handled) during the first 14 days of life. We found that, in comparison with their handled counterparts, maternally separated and non-handled animals are hyperactive when placed in a novel setting, display a dose-dependent higher sensitivity to cocaine-induced locomotor activity and respond to a mild stressor (tail-pinch) with significantly greater increases in nucleus accumbens dopamine levels. In addition, maternally separated animals were found to sensitize to the locomotor stimulant action of amphetamine when repeatedly stressed under conditions that failed to sensitize handled and non-handled animals. Finally, quantitative receptor autoradiography revealed a lower density of nucleus accumbens-core and striatal dopamine transporter sites in maternally separated animals. Interestingly, we also found greatly reduced D(3) dopamine receptor binding and mRNA levels in the nucleus accumbens-shell of handled animals. Together, these findings provide compelling evidence that disruptions in early postnatal rearing conditions can lead to profound and lasting changes in the responsiveness of mesocorticolimbic dopamine neurons to stress and psychostimulants, and suggest a neurobiological basis for individual differences in vulnerability to compulsive drug taking.

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Strain of foster mother determines long-term effects of early handling: Evidence for maternal mediation

Cited by 22 publications

References 37 publications

The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat

The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat

Sensitization of depressive-like behavior during repeated maternal separation is associated with more-rapid increase in core body temperature and reduced plasma cortisol levels

Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats

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