Translational Relevance of Rodent Models of Hypothalamic-pituitary-adrenal Function and Stressors in Adolescence

Overview

Journal Neurobiol Stress

Date 2017 Feb 24

PMID 28229107

Citations 27

Authors

Cheryl M McCormick

Matthew R Green

Jonathan J Simone

Affiliations

Soon will be listed here.

Abstract

Elevations in glucocorticoids that result from environmental stressors can have programming effects on brain structure and function when the exposure occurs during sensitive periods that involve heightened neural development. In recent years, adolescence has gained increasing attention as another sensitive period of development, a period in which pubertal transitions may increase the vulnerability to stressors. There are similarities in physical and behavioural development between humans and rats, and rats have been used effectively as an animal model of adolescence and the unique plasticity of this period of ontogeny. This review focuses on benefits and challenges of rats as a model for translational research on hypothalamic-pituitary-adrenal (HPA) function and stressors in adolescence, highlighting important parallels and contrasts between adolescent rats and humans, and we review the main stress procedures that are used in investigating HPA stress responses and their consequences in adolescence in rats. We conclude that a greater focus on timing of puberty as a factor in research in adolescent rats may increase the translational relevance of the findings.

Citing Articles

Hemispheric asymmetries and network dysfunctions in adolescent depression: A neuroimaging study using resting-state functional magnetic resonance imaging.

Xiong Y, Yu R, Wang X, Liang S, Ran J, Li X World J Psychiatry. 2025; 15(2):102412.

PMID: 39974491 PMC: 11758046. DOI: 10.5498/wjp.v15.i2.102412.

Beyond fur color: differences in socio-emotional behavior and the oxytocin system between male BL6 and CD1 mice in adolescence and adulthood.

Gryksa K, Schafer T, Gareis F, Fuchs E, Royer M, Schmidtner A Front Neurosci. 2024; 18:1493619.

PMID: 39717700 PMC: 11663876. DOI: 10.3389/fnins.2024.1493619.

Practical solutions for including sex as a biological variable (SABV) in preclinical neuropsychopharmacological research.

Dalla C, Jaric I, Pavlidi P, Hodes G, Kokras N, Bespalov A J Neurosci Methods. 2023; 401:110003.

PMID: 37918446 PMC: 10842858. DOI: 10.1016/j.jneumeth.2023.110003.

Impact of stress on excitatory and inhibitory markers of adolescent cognitive critical period plasticity.

Perica M, Luna B Neurosci Biobehav Rev. 2023; 153:105378.

PMID: 37643681 PMC: 10591935. DOI: 10.1016/j.neubiorev.2023.105378.

The gut microbiota, HPA axis, and brain in adolescent-onset depression: Probiotics as a novel treatment.

Freimer D, Yang T, Ho T, Tymofiyeva O, Leung C Brain Behav Immun Health. 2022; 26:100541.

PMID: 36536630 PMC: 9758412. DOI: 10.1016/j.bbih.2022.100541.

References

Kaplowitz E, Savenkova M, Karatsoreos I, Romeo R . Somatic and Neuroendocrine Changes in Response to Chronic Corticosterone Exposure During Adolescence in Male and Female Rats. J Neuroendocrinol. 2015; 28(2):12336. DOI: 10.1111/jne.12336. View

Lussier A, Caruncho H, Kalynchuk L . Repeated exposure to corticosterone, but not restraint, decreases the number of reelin-positive cells in the adult rat hippocampus. Neurosci Lett. 2009; 460(2):170-4. DOI: 10.1016/j.neulet.2009.05.050. View

McCormick C, Smith C, Mathews I . Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res. 2007; 187(2):228-38. DOI: 10.1016/j.bbr.2007.09.005. View

Taylor S, Taylor A, Koenig J . The interaction of disrupted type II neuregulin 1 and chronic adolescent stress on adult anxiety- and fear-related behaviors. Neuroscience. 2012; 249:31-42. PMC: 3568180. DOI: 10.1016/j.neuroscience.2012.09.045. View

Lukkes J, Norman K, Meda S, Andersen S . Sex differences in the ontogeny of CRF receptors during adolescent development in the dorsal raphe nucleus and ventral tegmental area. Synapse. 2015; 70(3):125-32. DOI: 10.1002/syn.21882. View

Mathews I, Mills R, McCormick C . Chronic social stress in adolescence influenced both amphetamine conditioned place preference and locomotor sensitization. Dev Psychobiol. 2008; 50(5):451-9. DOI: 10.1002/dev.20299. View

Bouma E, Riese H, Ormel J, Verhulst F, Oldehinkel A . Adolescents' cortisol responses to awakening and social stress; effects of gender, menstrual phase and oral contraceptives. The TRAILS study. Psychoneuroendocrinology. 2009; 34(6):884-93. DOI: 10.1016/j.psyneuen.2009.01.003. View

Hetzel A, Rosenkranz J . Distinct effects of repeated restraint stress on basolateral amygdala neuronal membrane properties in resilient adolescent and adult rats. Neuropsychopharmacology. 2014; 39(9):2114-30. PMC: 4104329. DOI: 10.1038/npp.2014.60. View

Marshall A . Developmental Timing of Trauma Exposure Relative to Puberty and the Nature of Psychopathology Among Adolescent Girls. J Am Acad Child Adolesc Psychiatry. 2015; 55(1):25-32.e1. PMC: 4691280. DOI: 10.1016/j.jaac.2015.10.004. View

10.

Vetter-OHagen C, Spear L . Hormonal and physical markers of puberty and their relationship to adolescent-typical novelty-directed behavior. Dev Psychobiol. 2011; 54(5):523-35. PMC: 3288810. DOI: 10.1002/dev.20610. View

11.

Ver Hoeve E, Kelly G, Luz S, Ghanshani S, Bhatnagar S . Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience. 2013; 249:63-73. PMC: 3743933. DOI: 10.1016/j.neuroscience.2013.01.073. View

12.

Buwalda B, Geerdink M, Vidal J, Koolhaas J . Social behavior and social stress in adolescence: a focus on animal models. Neurosci Biobehav Rev. 2010; 35(8):1713-21. DOI: 10.1016/j.neubiorev.2010.10.004. View

13.

Qiao H, Li M, Xu C, Chen H, An S, Ma X . Dendritic Spines in Depression: What We Learned from Animal Models. Neural Plast. 2016; 2016:8056370. PMC: 4736982. DOI: 10.1155/2016/8056370. View

14.

Conrad C, MacMillan 2nd D, Tsekhanov S, Wright R, Baran S, Fuchs R . Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning. Neurobiol Learn Mem. 2004; 81(3):185-99. DOI: 10.1016/j.nlm.2004.01.002. View

15.

Zhang J, Lam S, Kong A, Ma R, Li S, Chan J . Family conflict and lower morning cortisol in adolescents and adults: modulation of puberty. Sci Rep. 2016; 6:22531. PMC: 4772378. DOI: 10.1038/srep22531. View

16.

van Haaster L, de Rooij D . Spermatogenesis is accelerated in the immature Djungarian and Chinese hamster and rat. Biol Reprod. 1993; 49(6):1229-35. DOI: 10.1095/biolreprod49.6.1229. View

17.

Lopez-Duran N, McGinnis E, Kuhlman K, Geiss E, Vargas I, Mayer S . HPA-axis stress reactivity in youth depression: evidence of impaired regulatory processes in depressed boys. Stress. 2015; 18(5):545-53. PMC: 5403248. DOI: 10.3109/10253890.2015.1053455. View

18.

McCormick C, Robarts D, Gleason E, Kelsey J . Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats. Horm Behav. 2004; 46(4):458-66. DOI: 10.1016/j.yhbeh.2004.05.004. View

19.

Parent A, Franssen D, Fudvoye J, Gerard A, Bourguignon J . Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: Revision of human observations and mechanistic insight from rodents. Front Neuroendocrinol. 2015; 38:12-36. DOI: 10.1016/j.yfrne.2014.12.004. View

20.

Kajantie E, Phillips D . The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology. 2005; 31(2):151-78. DOI: 10.1016/j.psyneuen.2005.07.002. View