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Development of Individual Differences in Behavioral and Endocrine Responses to Stress: Role of the Postnatal Environment

Christian Caldji, Dong Liu, Shakti Sharma, Josie Diorio, Darlene Francis, Michael J. Meaney, Paul M. Plotsky

10.1002/cphy.cp070413

Source: Supplement 23: Handbook of Physiology, The Endocrine System, Coping with the Environment: Neural and Endocrine Mechanisms

Originally published: 2001

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Hypothalamic‐Pituitary‐Adrenal Stress Response
2 Environmental Regulation of Hypothalamic‐Pituitary‐Adrenal Development
2.1 Effects of Handling (or Infantile Stimulation)
2.2 Effects of Prolonged Periods of Maternal Separation
2.3 Effects of Neonatal Endotoxin Exposure
3 Summary of Early Environmental Effects
3.1 Effects of Handling on Chronic Responses to Stress
3.2 Acute Stress Responses in Handled and Nonhandled Rats: Revisited
4 Summary
5 Biological Significance
6 Early Environmental Effects: The Levine Maternal Mediation Hypothesis
6.1 Stability of Individual Differences in Maternal Behavior
6.2 Transmission of Individual Differences in Maternal Care to Offspring
6.3 Mode of Transmission: Genomic or Nongenomic?
7 Conclusions
Figure 1. Figure 1.

Integrates plasma corticotropin (ACTH) responses [pg/ (ml · min)] to restraint stress in handled (H) and nonhandled (NH) rats that were adrenalectomized (ADX), adrenalectomized and given basal levels of corticosterone replacement ADX+B), or shamoperated controls (SHAM). *Nonhandled values which differ at P < 0.05 from those handled animals.
Figure 2. Figure 2.

A summary of our earlier understanding of the mechanisms underlying the differences in hypothalamic‐pituitary‐adrenal responses to acute stress in handled and nonhandled animals. Increased glucocorticoid receptor (Grec) levels confer greater sensitivity to cotricosterone (B) in hippocampal tissue from handled animals. Therefore, even under basal corticosterone levels (which do not differ between young and adult handled or nonhandled rats) there is a greater tonic inhibitory signal (‐) on hypothalamic corticotropin‐releasing factor (CRF) and arginine vasopressin (AVP) synthesis in handled rats. In response to the neural signals associated with stress and impinging on the hypothalamus, there is greater release of CRF and AVP into the portal circulation (+) in nonhandled rats, resulting in greater corticotropin (ACTH) release.
Figure 3. Figure 3.

Two related models that might explain in part, conditions where Handled and Nonhandled rats differ in hypothalamic‐pituitary‐adrenal (HPA) responses to acute stress. These neural models involves sites responsible for dynamic regulation of Corticotropin‐releasing factor (CRF) and arginine vasopresin (AVP) synthesis and release; some of these sites are sensitive to glucocorticoid (GC) feedback inhibition and to the facilitatory effects of chronic stress, and others are not. In addition, glucocorticoid feedback serves as a signal for tonic inhibition of CRF and AVP synthesis under resting‐state conditions. Finally, we propose an active inhibitory site that monitors the novelty of a stimulus. This site is active under conditions where a stimulus is familiar to the animal. Thus, HPA responses to novel stressors should exceed those occurring in response to familiar stressors. This site is concerned only with the aspect of novelty and does not eliminate the HPA response, except under conditions where the original response occurred due only to the novelty of the stimulus. A: These influences are exerted directly upon release from paraventricular (PVN) neurons. B: The effect occurs at sites which, in turn, stimulate release from PVN neurons. These are not mutually exclusive possibilities. NA, noradrenaline.


Figure 1.

Integrates plasma corticotropin (ACTH) responses [pg/ (ml · min)] to restraint stress in handled (H) and nonhandled (NH) rats that were adrenalectomized (ADX), adrenalectomized and given basal levels of corticosterone replacement ADX+B), or shamoperated controls (SHAM). *Nonhandled values which differ at P < 0.05 from those handled animals.



Figure 2.

A summary of our earlier understanding of the mechanisms underlying the differences in hypothalamic‐pituitary‐adrenal responses to acute stress in handled and nonhandled animals. Increased glucocorticoid receptor (Grec) levels confer greater sensitivity to cotricosterone (B) in hippocampal tissue from handled animals. Therefore, even under basal corticosterone levels (which do not differ between young and adult handled or nonhandled rats) there is a greater tonic inhibitory signal (‐) on hypothalamic corticotropin‐releasing factor (CRF) and arginine vasopressin (AVP) synthesis in handled rats. In response to the neural signals associated with stress and impinging on the hypothalamus, there is greater release of CRF and AVP into the portal circulation (+) in nonhandled rats, resulting in greater corticotropin (ACTH) release.



Figure 3.

Two related models that might explain in part, conditions where Handled and Nonhandled rats differ in hypothalamic‐pituitary‐adrenal (HPA) responses to acute stress. These neural models involves sites responsible for dynamic regulation of Corticotropin‐releasing factor (CRF) and arginine vasopresin (AVP) synthesis and release; some of these sites are sensitive to glucocorticoid (GC) feedback inhibition and to the facilitatory effects of chronic stress, and others are not. In addition, glucocorticoid feedback serves as a signal for tonic inhibition of CRF and AVP synthesis under resting‐state conditions. Finally, we propose an active inhibitory site that monitors the novelty of a stimulus. This site is active under conditions where a stimulus is familiar to the animal. Thus, HPA responses to novel stressors should exceed those occurring in response to familiar stressors. This site is concerned only with the aspect of novelty and does not eliminate the HPA response, except under conditions where the original response occurred due only to the novelty of the stimulus. A: These influences are exerted directly upon release from paraventricular (PVN) neurons. B: The effect occurs at sites which, in turn, stimulate release from PVN neurons. These are not mutually exclusive possibilities. NA, noradrenaline.

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Article Title: Development of Individual Differences in Behavioral and Endocrine Responses to Stress: Role of the Postnatal Environment
 

How to Cite

Christian Caldji, Dong Liu, Shakti Sharma, Josie Diorio, Darlene Francis, Michael J. Meaney, Paul M. Plotsky. Development of Individual Differences in Behavioral and Endocrine Responses to Stress: Role of the Postnatal Environment. Compr Physiol 2011, Supplement 23: Handbook of Physiology, The Endocrine System, Coping with the Environment: Neural and Endocrine Mechanisms: 271-292. First published in print 2001. doi: 10.1002/cphy.cp070413