The link between aberrant hypothalamic–pituitary–adrenal axis activity during development and the emergence of aggression—Animal studies

Walker, Sophie E.; Papilloud, Aurélie; Huzard, Damien; Sandi, Carmen

doi:10.1016/j.neubiorev.2016.10.008

Cited by 49Stress Responses and CortisolNeuroendocrine regulation and behaviorBullying, Victimization, and Aggression

The link between aberrant hypothalamic–pituitary–adrenal axis activity during development and the emergence of aggression—Animal studies

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Walker, Sophie E., Papilloud, Aurélie, Huzard, Damien, Sandi, Carmen·2018·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2016.10.008

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Abstract

Aggressive behavior is not uniform, including proactive and reactive forms of aggression. Aberrant functioning of the hypothalamic-pituitary-adrenal (HPA) axis is frequently associated with abnormal aggression. Here, we review the rodent literature in order to assess whether developmental abnormalities in the HPA axis can be causally linked with the emergence of abnormal aggression. We examine studies that involve genetic models and life challenges (e.g., early life stress, drug exposure) that course with developmental alterations in the HPA axis. Although the lack of systematic studies hinders development of an integrated model, existing evidence supports a U-shaped function regarding differences in HPA axis functioning during development and the emergence of aggressive phenotypes. Thus, developmentally low or high HPA axis reactivity are typically found to be aligned with the emergence of aggressive phenotypes; however, existing information is insufficient to causally link divergent HPA axis aberration with specific types of aggression. Progress in this field is needed to support interventions in children aimed at ameliorating social dysfunctions associated with aberrations in HPA axis function.

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Animal studies have consistently shown a robust association between the HPA axis and aggressive behavior.
“Animal studies have consistently shown a robust association between the HPA axis and aggressive behavior [98].”
From Genetics of child aggression, a systematic review (2024) · cites this paper as [98]

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Sandman (1999) · doi:10.1002/(sici)1098-2302(199904)34:3

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Maladaptive Aggression: With a Focus on Impulsive Aggression in Children and Adolescents
Connor, D. F., Newcorn, J. H., Saylor, K. E., Amann, B. H., Scahill, L. D., Robb, A. S., Jensen, P. S., Vitiello, B., Findling, R. L., & Buitelaar, J. K. (2019) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2019.0039 · Cited by 82 · see citing works
“In turn, these regulate the hypothalamic-pituitary-adrenal (HPA) stress response system (Walker et al. 2018).”
Background
Perinatal fluoxetine effects on social play, the HPA system, and hippocampal plasticity in pre-adolescent male and female rats: Interactions with pre-gestational maternal stress
Gemmel, M., Hazlett, M. F., Bögi, E., Lacalle, S. D., Hill, L. A., Kokras, N., Hammond, G. L., Dalla, C., Charlier, T. D., & Pawluski, J. L. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.07.480 · Cited by 56 · see citing works
Constitutive differences in glucocorticoid responsiveness to stress are related to variation in aggression and anxiety-related behaviors
Walker, S. E., Zanoletti, O., Guillot de Suduiraut, I., & Sandi, C. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.011 · Cited by 40 · see citing works
Self-citation
Perinatal fluoxetine has enduring sexually differentiated effects on neurobehavioral outcomes related to social behaviors
Gemmel, M., Lacalle, S. D., Mort, S. C., Hill, L. A., Charlier, T. D., & Pawluski, J. L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.10.009 · Cited by 39 · see citing works
“, 2012b), a system that has been linked to social interactions and aggressive phenotypes (Walker et al., 2016).”
Genetics of child aggression, a systematic review
Koyama, E., Kant, T., Takata, A., Kennedy, J. L., & Zai, C. C. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02870-7 · Cited by 33 · see citing works
Low vagal tone in two rat models of psychopathology involving high or low corticosterone stress responses
Huzard, D., Ghosal, S., Grosse, J., Carnevali, L., Sgoifo, A., & Sandi, C. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.11.003 · Cited by 32 · see citing works
Self-citation
Non-angry aggressive arousal and angriffsberietschaft: A narrative review of the phenomenology and physiology of proactive/offensive aggression motivation and escalation in people and other animals
Potegal, M., & Nordman, J. C. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105110 · Cited by 30 · see citing works
“The term “under-aroused” has also been applied to the proactively aggressive and sometimes psychopathic individuals construed to be human counterparts of HPA down-regulated rats, although the presumption of equivalence must be evaluated against the multiple and complex, time, sex and experience-dependent effects found…”
Long-term programing of psychopathology-like behaviors in male rats by peripubertal stress depends on individual’s glucocorticoid responsiveness to stress
Walker, S. E., & Sandi, C. (2018) · Stress · doi:10.1080/10253890.2018.1435639 · Cited by 30 · see citing works
Self-citation
Experience and activity-dependent control of glucocorticoid receptors during the stress response in large-scale brain networks
Huzard, D., Rappeneau, V., Meijer, O. C., Touma, C., Arango-Lievano, M., Garabedian, M. J., & Jeanneteau, F. D. (2020) · Stress · doi:10.1080/10253890.2020.1806226 · Cited by 23 · see citing works
“Studies with rats, selected for low, intermediate and high glucocorticoid responsivity to stress, distinguish subjects based on singular coping strategies in response to various challenges (Huzard et al., 2019; Walker et al., 2018; Walker et al., 2017).”
BackgroundSelf-citation
Alterations in brain microstructure in rats that develop abnormal aggression following peripubertal stress
Walker, S. E., Wood, T., Cash, D., Mesquita, M. S., Williams, S., & Sandi, C. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14061 · Cited by 25 · see citing works
Self-citation
Peripubertal stress following maternal immune activation sex-dependently alters depression-like behaviors in offspring
Ranaei, E., Torshizi, S., Amini, A., Heidari, M. H., Namvarpour, Z., Fathabady, F. F., & Salari, A. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112800 · Cited by 24 · see citing works
The Relationship between Canine Behavioral Disorders and Gut Microbiome and Future Therapeutic Perspectives
Kiełbik, P., & Witkowska‐Piłaszewicz, O. (2024) · Animals · doi:10.3390/ani14142048 · Cited by 24 · see citing works
“The HPA axis is the main physiological system that modulates a wide variety of behavioral processes, especially body stress response, but also rewarding behaviors, learning, and memory [156–158].”
Background
Regulation of aggressive behaviors by nicotinic acetylcholine receptors: Animal models, human genetics, and clinical studies
Lewis, A. S., & Picciotto, M. R. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107929 · Cited by 23 · see citing works
miR-212 mediates counter-regulation on CRH expression and HPA axis activity in male mice
Tang, Y., Cai, X., Zhang, H., Shen, H., Wang, W., Shen, Z., Gu, W., Ling, C., & Li, M. (2017) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0124 · Cited by 21 · see citing works
Horse welfare: A joint assessment of four categories of behavioural indicators using the AWIN protocol, scan sampling and surveys
Ruet, A., Arnould, C., Lemarchand, J., Parias, C., Mach, N., Moisan, M., Foury, A., Briant, C., & Lansade, L. (2022) · Animal Welfare · doi:10.7120/09627286.31.3.008 · Cited by 18 · see citing works
Exploring the influence of stress on aggressive behavior and sexual function: Role of neuromodulator pathways and epigenetics
Mbiydzenyuy, N. E., Hemmings, S. M. J., Shabangu, T. W., & Qulu-Appiah, L. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e27501 · Cited by 21 · see citing works
Gut-Brain Axis: Probiotic,<i>Bacillus subtilis</i>, Prevents Aggression via the Modification of the Central Serotonergic System
Cheng, H.-W., Jiang, S., & Hu, J. (2019) · Oral Health by Using Probiotic Products · doi:10.5772/intechopen.86775 · Cited by 17 · see citing works
Targeting the Endocannabinoid System in Borderline Personality Disorder: Corticolimbic and Hypothalamic Perspectives
Ferber, S. G., Hazani, R., Shoval, G., & Weller, A. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200429234430 · Cited by 16 · see citing works
“More accurately, a brain-circuit comprising the amygdala, hypothalamus, and periaqueductal gray has been identified in a growing body of literature; heightened activation of this circuit may set off reactive aggression [64-66].”
Background
Coping styles vary with species’ sociality and life history: A systematic review and meta-regression analysis
Duckworth, R. A., Chenard, K. C., Meza, L. A., & Beiriz, M. C. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105241 · Cited by 14 · see citing works
“…causes consistent individual variation in behavioral traits is unknown, although direct effects have been suggested for studies of developmental influences on aggression (Ahmed et al., 2014; Aubin-Horth et al., 2012; Walker et al., 2018) and anxiety (de Kloet et al., 2004; Welberg and Seckl, 2001).”
Background
Domestication Explains Two-Thirds of Differential-Gene-Expression Variance between Domestic and Wild Animals; The Remaining One-Third Reflects Intraspecific and Interspecific Variation
Витальевна, Ч. И., Ponomarenko, P. M., Kozhemyakina, R. V., Suslov, V. V., Bogomolov, A. G., Klimova, N. V., Шихевич, С. Г., Savinkova, L. K., Oshchepkov, D. Y., Kolchanov, N. A., et al. (2021) · Animals · doi:10.3390/ani11092667 · Cited by 14 · see citing works
Association of mineralocorticoid receptor gene (NR3C2) hypermethylation in adult males with aggressive behavior
Qing, L., Gao, C., Ji, A., Lü, X., Zhou, L., & Nie, S. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112980 · Cited by 12 · see citing works
Glucocorticoids and Aggression: A Tripartite Interaction
Haller, J. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2022_307 · Cited by 11 · see citing works
Review: Suicide and its relationship to aggression and impulsivity
Lee, Y., Gilbert, J. R., Waldman, L. R., Zarate, C. A., & Ballard, E. D. (2025) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-025-01321-0 · Cited by 14 · see citing works
“However, the direction of the association between HPA axis activity, aggression, and impulsivity is complicated, particularly when considering developmental factors (Gollan et al., 2005; Walker et al., 2018), suggesting a nonlinear relationship.”
Postweaning stress affects behavior, brain and gut microbiota of adolescent mice in a sex-dependent manner
Yin, X., Zhao, Y., Wang, S., Feng, H., He, X., Li, X., Liu, X., Lu, H., Wen, D., Shi, Y., et al. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109869 · Cited by 10 · see citing works
A Rat Model of Human Behavior Provides Evidence of Natural Selection Against Underexpression of Aggressiveness-Related Genes in Humans
Oshchepkov, D. Y., Ponomarenko, M. P., Klimova, N. V., Витальевна, Ч. И., Олегович, Б. А., Sharypova, E. B., Шихевич, С. Г., & Kozhemyakina, R. V. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.01267 · Cited by 10 · see citing works
The Influence of Cecal Microbiota Transplantation on Chicken Injurious Behavior: Perspective in Human Neuropsychiatric Research
Fu, Y., & Cheng, H. W. (2024) · Biomolecules · doi:10.3390/biom14081017 · Cited by 10 · see citing works
“Although there are dissimilarities between humans and chickens, the brain neural circuitries for aggression and social behavior appear to be evolutionarily conserved across the vertebrates [18,108,109].”
Background
The dexamethasone suppression test as a biomarker for suicidal behavior: A systematic review and meta-analysis
Spaan, P., Verrijp, T., Michielsen, P. J. S., Birkenhäger, T. K., Hoogendijk, W. J. G., & Roza, S. J. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.09.048 · Cited by 7 · see citing works
Relationship between heart rate variability and aggressive behavior among patients with schizophrenia hospitalized in acute wards
Wang, H., Yang, C., Chen, K., & Chueh, K. (2019) · Perspectives In Psychiatric Care · doi:10.1111/ppc.12433 · Cited by 7 · see citing works
Callous unemotional trait-like mice and their stressed dams
Giovanni Laviola, A., Leonardo, A., Ceci, F. M., & Fiore, M. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105296 · Cited by 7 · see citing works
Long-Term Soft-Food Rearing in Young Mice Alters Brain Function and Mood-Related Behavior
Furukawa, M., Tada, H., Raju, R., Wang, J., Yokoi, H., Yamada, M., Shikama, Y., & Matsushita, K. (2023) · Nutrients · doi:10.3390/nu15102397 · Cited by 5 · see citing works
“Furthermore, these brain regions play a role in regulating the hypothalamus-pituitary-adrenal stress response system [75].”
Background
Transcriptomic signature related to poor welfare of sport horses
Foury, A., Mach, N., Ruet, A., Lansade, L., & Moisan, M. (2023) · Comprehensive Psychoneuroendocrinology · doi:10.1016/j.cpnec.2023.100201 · Cited by 5 · see citing works
“Although a causal link between aberrant hypothalamic-pituitary-adrenal (HPA) axis and aggressiveness has not been proved so far, developmentally low or high HPA axis reactivity is typically found to be aligned with the emergence of aggressive phenotypes [64].”
Background
Elevated aggressive behavior in male mice with thyroid-specific Prkar1a and global Epac1 gene deletion
Russart, K. L. G., Huk, D. J., Nelson, R. J., & Kirschner, L. S. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.12.012 · Cited by 5 · see citing works
“, 2012), and either low or high activity of the HPA can induce aggression (Walker et al., 2016).”
The impact of early life stress and schizophrenia on motor and cognitive functioning: an experimental study
Oginga, F. O., & Mpofana, T. (2023) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2023.1251387 · Cited by 5 · see citing works
Juvenile adversity and adult threat controllability in translational models of stress-related disorders
Ritov, G., Ardi, Z., Horovitz, O., Albrecht, A., & Richter‐Levin, G. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.02.006 · Cited by 5 · see citing works
Proopiomelanocortin (POMC) is a negative regulator of tadpole aggression through opioid receptor signalingPreprint
McKinney, J. E., Ludington, S. C., Butler, J. M., & O’Connell, L. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.28.518266 · Cited by 4 · see citing works
Low emotional contagious behavior induces PTSD susceptibility in observers and is related to the regulation of oxytocin receptor in mice
Liu, Y., Gao, Y., Ma, Z., Zhang, Q., Sun, R., Wang, L., Zhao, S., Li, C., Lian, B., Sun, H., et al. (2025) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-024-01244-2 · Cited by 3 · see citing works
“Low response levels in the HPA axis often characterize apa-thy and indifference (Walker et al., 2018).”
Repeated Experience of Aggression Changes in Gene Expression in the Hypothalamus in Male Mice of Two Strains
Sapronova, A. A., Kisaretova, P. E., Salman, R., & Bondar, N. P. (2023) · Neurochemical Journal · doi:10.1134/s1819712423030169 · Cited by 2 · see citing works
The Biology of Glucocorticoids: Normal and Abnormal Aggression
Haller, J. (2020) · Springer eBooks · doi:10.1007/978-3-030-46331-1_5 · Cited by 1 · see citing works
Neonatal action of the dipeptidyl peptidase iv inhibitor diprotin A leads to a hyperactive phenotype formation and a prolonged increase in aggressiveness in rats
Khlebnikova, N. N., Ширенова, С. Д., & Krupina, N. A. (2021) · Zhurnal «Patologicheskaia fiziologiia i eksperimental`naia terapiia» · doi:10.25557/0031-2991.2021.04.4-16
Glucocorticoids in Humans
Haller, J. (2020) · Springer eBooks · doi:10.1007/978-3-030-46331-1_6
Editorial: Jeffrey Glennon & Simone Macrì
(2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.032
Repeated Experience of Aggression Changes Gene Expression in Hypothalamus in Male Mice of Two Strains
Sapronova, A. A., Kisaretova, P. E., Salman, R., & Bondar, N. P. (2023) · Нейрохимия · doi:10.31857/s1027813323030160
Serum Levels of Cortisol and Testosterone in American Mink (Neogale Vison) Selected for Aggressive and Tame Behavior towards Humans
Panova, E., Калинина, С. Н., Ilyukha, V. A., Васильевич, Т. О., Балан, О. В., Nekrasova, M., & Stepanova, M. A. (2024) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093024040136
Is Aggression Normal in Humans?
Pop-Jordanova, N. D. (2025) · PRILOZI · doi:10.2478/prilozi-2025-0001
Association between exposure to ambient particulate matter and aggression among adolescents: a national school-based study in China
Hu, J., Hu, W., Xu, Z., Peng, C., Cheng, J., Rong, F., Wang, Y. C., Zhang, N., Guan, M., Wei, J., et al. (2025) · BMC Public Health · doi:10.1186/s12889-025-25023-x
“Thirdly, PM such as PM 2.5 may induce hypothalamic-pituitary-adrenal (HPA)-axis action, which may contribute to the onset of aggression [44, 45].”
Influential
Prolonged Aggressive Experience Accelerates Resolution of Inflammation in Blood and Microglia After Repeated LPS Treatment
Mutovina, A., Sapronova, A., Ayriyants, K. A., Ryabushkina, Y. A., Khantakova, J. N., Mezhevalova, P., Ritter, P., & Bondar, N. P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262412007
“Consistent with our findings, other studies report no GR expression changes in the hypothalamus of highly aggressive rats [45], hippocampus of aggression-selected rats [76], or GR protein levels across brain regions [80].”
Altération de l’état de bien-être du cheval domestique : effets de pratiques d’hébergement liées au box individuel et relations avec l’équitation
Ruet, A. (2020) · doi:10.70675/70b1b54dzf824z4086z96ebz1a0a35763a6b
Traumatic life experiences during critical periods lead to diverse developmental trajectories
Morelli, G., Visintin, G., Gelli, E., Serani, A., Bartolucci, M., Uccella, S., D’APRUZZO, M., Preiti, D., Chellali, M. M., Cucinelli, A., et al. (2026) · Cell Reports Medicine · doi:10.1016/j.xcrm.2026.102798
Postweaning swimming exercise attenuates maternal sleep deprivation-induced aggressive behavior in offspring mice
Yu, X., Zhou, F., Gong, M., Li, X., Liu, X., He, X., Li, Y., Sang, Y., Yin, X., Liu, X. Y., et al. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116292

Stress and aggression
Böhnke, R. (2010) · Universitätsbibliothek Trier · doi:10.25353/ubtr-xxxx-5e48-73ac
Stress and Aggression - a psychophysiological approach
Böhnke, R. (2010) · Hochschulschriftenserver der Universität Trier (Universität Trier)
Die Verwendung von Mischverteilungsmodellen zur Optimierung wiederholter Erhebungen in Patientenorientierter Versorgungsforschung und psychotherapeutischer Praxis
Böhnke, J. R. (2013) · Hochschulschriftenserver der Universität Trier (Universität Trier) · doi:10.25353/ubtr-xxxx-64ee-f954
Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: What can we learn from animal models?
Veenema, A. H. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.003 · Cited by 268 · see citing works
The relationship between basal and acute HPA axis activity and aggressive behavior in adults
Böhnke, R., Bertsch, K., Kruk, M. R., & Naumann, E. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0391-x · Cited by 86 · see citing works

Authors: Walker, S. E., Papilloud, A., Huzard, D., & Sandi, C.
Affiliations: École Polytechnique Fédérale de Lausanne (CH)
Corresponding author: Sandi, Carmen
ORCID: Walker, Sophie E.
Papilloud, Aurélie
Huzard, Damien
Sandi, Carmen
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2018-08
Volume: 91
Pages: 138-152
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2016.10.008
OpenAlex: W2535720182
Cited by: 49
References: 198
Citations by year: 2026: 2 · 2025: 5 · 2024: 7 · 2023: 7 · 2022: 3 · 2021: 3 · 2020: 7 · 2019: 5 · 2018: 6 · 2017: 4
FWCI: 0.51
Type: journal article
Language: en
Open access: bronze
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doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Neuroscience & Biobehavioral Reviews (acceptedVersion)
PubMed (publishedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders: European Union’s Seventh Framework Programme (603016)
Oak Foundation
Swiss National Science Foundation (31003A-152614)
EPFL
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Social Sciences › Psychology › Social Psychology › Bullying, Victimization, and Aggression
Keywords: hypothalamic-pituitary-adrenal axis, aggression, proactive aggression, reactive aggression, early life stress, developmental programming, HPA axis reactivity, genetic models, drug exposure, rodent models, social dysfunction, children
MeSH terms: Aggression, Animals, Behavior, Animal, Hypothalamo-Hypophyseal System, Pituitary-Adrenal System, Stress, Psychological, Models, Animal

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The link between aberrant hypothalamic–pituitary–adrenal axis activity during development and the emergence of aggression—Animal studies

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