The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course

McEwen, Bruce S.; Morrison, John H.

doi:10.1016/j.neuron.2013.06.028

Cited by 1,079Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology Studies

The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course

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McEwen, Bruce S., Morrison, John H.·2013·Neuron

DOI 10.1016/j.neuron.2013.06.028PMC PMC3753223

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Abstract

The prefrontal cortex (PFC) is involved in working memory and self-regulatory and goal-directed behaviors and displays remarkable structural and functional plasticity over the life course. Neural circuitry, molecular profiles, and neurochemistry can be changed by experiences, which influence behavior as well as neuroendocrine and autonomic function. Such effects have a particular impact during infancy and in adolescence. Behavioral stress affects both the structure and function of PFC, though such effects are not necessarily permanent, as young animals show remarkable neuronal resilience if the stress is discontinued. During aging, neurons within the PFC become less resilient to stress. There are also sex differences in the PFC response to stressors. While such stress and sex hormone-related alterations occur in regions mediating the highest levels of cognitive function and self-regulatory control, the fact that they are not necessarily permanent has implications for future behavior-based therapies that harness neural plasticity for recovery.

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In rodents, the most abundant and consistent changes in chronic stress models are in the medial prefrontal cortex, including anterior cingulate, prelimbic, and infralimbic regions, with somewhat more variable, mixed direction effects in the orbitofrontal cortex.
“In rodents, the most abundant and consistent changes are in the mPFC (anterior cingulate, prelimbic and infralimbic) with somewhat more variable, mixed direction effects in the OFC (Fig. 3, top left-hand panel).”
From Prefrontal cortex and depression (2022) · cites this paper as [98]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Accompanying behavioral changes in chronic stress models are marked physiological and structural alterations in the amygdala, hippocampus, and prefrontal cortex that are similar to those seen in major depressive disorder.
“Accompanying these behavioral changes are marked physiological and structural alterations, not only in the amygdala and hippocampus but, importantly, the PFC [98,99], that are similar to those seen in MDD.”
From Prefrontal cortex and depression (2022) · cites this paper as [98]
The “Effects of Stress on Prefrontal Cortex” section says repeated stress causes functional and structural changes in the PFC, amygdala, and hippocampus. “Relevance to human vulnerabilities and potential for brain plasticity” describes frontal-cortex and hippocampal changes in depressed individuals, but does not establish that the alterations across all three regions are similar to those in MDD. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The PFC likely regulates play in a multifactorial manner, contributing to expression of the behavior through its roles in suppressing aggression, monitoring approach/avoid conflict, and modulating the stress response via its projections to the MeA and other stress-modulatory nodes.
“The PFC likely regulates play in a multifactorial manner, contributing to expression of the behavior through its roles in suppressing aggression, monitoring approach/avoid conflict, and modulating the stress response via its projections to the MeA and other stress-modulatory nodes (Aupperle & Paulus, 2010; McEwen & Morrison, 2013; Takahashi et al., 2014).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as McEwen & Morrison, 2013
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Stress-induced structural changes in the PFC contribute to the pathophysiology of neuropsychiatric conditions.
“Although stress-induced structural changes in the PFC are equally important in their contribution to the pathophysiology of neuropsychiatric conditions [256–262]”
From Development of prefrontal cortex (2022) · cites this paper as [261]
Overwhelming evidence indicates PFC is uniquely important brain region for highest level of executive function, which drives self-regulatory and goal-directed behaviors.
“Overwhelming evidence has indicated that PFC is a uniquely important brain region for the highest level of excecutive function, which drives self-regulatory and goal-directed behaviors 261–263.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [261]

Chronic stress exposure increases the risk of developing various neuropsychiatric illnesses.
“Chronic stress exposure increases the risk of developing various neuropsychiatric illnesses.”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [1]
Profound sensory experiences even in later life can significantly impact neural circuits, which in turn can recondition behavior.
“However, profound sensory experiences even in later life can significantly impact circuits, which in turn can recondition behavior5,6.”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [5]
Major emotional or psychological episodes like chronic stress, trauma, and drug addiction can alter brain function and behavior even much later in life.
“On the other hand, major emotional or psychological episodes like chronic stress, trauma, drug addiction can alter brain function and behavior even much later in life5,6.”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [5]
Induced plasticity under psychological, emotional or stressful conditions like PTSD, depression, social isolation or drug addiction is believed to elicit significant cellular re-adaptations in PFC leading to long term behavioral changes.
“induced plasticity under psychological, emotional or stressful conditions like PTSD, depression, social isolation or drug addiction is believed to elicit significant cellular re-adaptations in PFC leading to long term behavioral changes5.”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [5]
The neural circuits in a healthy brain are remodeled by experiences to enable behavioral responses appropriate to what the individual is experiencing.
“The neural circuits in a healthy brain are remodeled by experiences to enable behavioral responses that are appropriate to what the individual is experiencing”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [9]
Chronic stress causes dendritic shrinkage not only in CA3 and dentate gyrus neurons of hippocampus but also in medial amygdala and medial prefrontal cortex, while dendrites in basolateral amygdala and orbitofrontal cortex expand with chronic stress.
“Chronic stress causes dendritic shrinkage not only in CA3 and dentate gyrus neurons of hippocampus but also in medial amygdala and mPFC, while dendrites in BlA and orbitofrontal cortex expand with chronic stress.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [9]

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Birrell JM Brown VJ 2000b Medial frontal cortex mediates perceptual attentional set shifting in the rat J Neurosci 20 4320 4324 10818167 PMC6772641
Drevets WC Price JL Simpson JR Jr Todd RD Reich T Vannier M Raichle ME 1997b Subgenual prefrontal cortex abnormalities in mood disorders Nature 386 824 827 9126739

Sorted by citations

The Neuroscience of Mindfulness Meditation
Tang, Y.-Y., Hölzel, B. K., & Posner, M. I. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn3916 · Cited by 2,889 · see citing works
Stress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex
McEwen, B. S., Nasca, C., & Gray, J. D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.171 · Cited by 1,574 · see citing works
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Mechanisms of stress in the brain
McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015) · Nature Neuroscience · doi:10.1038/nn.4086 · Cited by 1,386 · see citing works
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Hallmarks of Brain Aging: Adaptive and Pathological Modification by Metabolic States
Mattson, M. P., & Arumugam, T. V. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.05.011 · Cited by 1,242 · see citing works
Time for united action on depression: a Lancet–World Psychiatric Association Commission
Herrman, H., Patel, V., Kieling, C., Berk, M., Buchweitz, C., Cuijpers, P., Furukawa, T. A., Kessler, R. C., Kohrt, B. A., Maj, M., et al. (2022) · The Lancet · doi:10.1016/s0140-6736(21)02141-3 · Cited by 1,104 · see citing works
Neurobiological and Systemic Effects of Chronic Stress
McEwen, B. S. (2017) · Chronic Stress · doi:10.1177/2470547017692328 · Cited by 1,059 · see citing works
“, being more vigilant and anxious in a potentially dangerous environment.(9) The healthy brain is resilient and neural circuitry adapts to a new situation along with underlying changes in gene expression.”
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Altered Connectivity in Depression: GABA and Glutamate Neurotransmitter Deficits and Reversal by Novel Treatments
Duman, R. S., Sanacora, G., & Krystal, J. H. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.013 · Cited by 1,026 · see citing works
Adolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Sex differences and stress across the lifespan
Bale, T. L., & Epperson, C. N. (2015) · Nature Neuroscience · doi:10.1038/nn.4112 · Cited by 751 · see citing works
Revisiting the Stress Concept: Implications for Affective Disorders
McEwen, B. S., & Akil, H. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0733-19.2019 · Cited by 686 · see citing works
“Adaptive plasticity is a term that describes how chronic stress can remodel the brain in a neuroprotective manner, causing retraction of dendrites and loss of synapses in areas that are highly stress sensitive, such as hippocampus, medial amygdala, and medial prefrontal cortex, while at the same time causing the expan…”
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Uncertainty and stress: Why it causes diseases and how it is mastered by the brain
Peters, A., McEwen, B. S., & Friston, K. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.004 · Cited by 652 · see citing works
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Prefrontal cortex and depression
Pizzagalli, D. A., & Roberts, A. C. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01101-7 · Cited by 644 · see citing works
Understanding the broad influence of sex hormones and sex differences in the brain
McEwen, B. S., & Milner, T. A. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23809 · Cited by 642 · see citing works
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How do antidepressants work? New perspectives for refining future treatment approaches
Harmer, C. J., Duman, R. S., & Cowen, P. J. (2017) · The Lancet Psychiatry · doi:10.1016/s2215-0366(17)30015-9 · Cited by 616 · see citing works
Pathogenesis of depression: Insights from human and rodent studies
Ménard, C., Hodes, G. E., & Russo, S. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.053 · Cited by 593 · see citing works
Early life stress and development: potential mechanisms for adverse outcomes
Smith, K. E., & Pollak, S. D. (2020) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-020-09337-y · Cited by 500 · see citing works
Risk factors for depression: an autobiographical review
Hammen, C. (2018) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050817-084811 · Cited by 483 · see citing works
Social Structure, Adversity, Toxic Stress, and Intergenerational Poverty: An Early Childhood Model
McEwen, C. A., & McEwen, B. S. (2017) · Annual Review of Sociology · doi:10.1146/annurev-soc-060116-053252 · Cited by 472 · see citing works
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Biological mechanisms underlying the role of physical fitness in health and resilience
Silverman, M. N., & Deuster, P. A. (2014) · Interface Focus · doi:10.1098/rsfs.2014.0040 · Cited by 416 · see citing works
Developmental Trajectories of Early Life Stress and Trauma: A Narrative Review on Neurobiological Aspects Beyond Stress System Dysregulation
Agorastos, A., Pervanidou, P., Chrousos, G. P., & Baker, D. G. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00118 · Cited by 385 · see citing works
“Interestingly, the distinct neural plasticity during development can lead to cortical adaptation with very specific regionally altered cortical representation fields (436, 437) and be potentially protecting from the specific sensory processing of different ELS/CT (417).”
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Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
Breath of Life: The Respiratory Vagal Stimulation Model of Contemplative Activity
Gerritsen, R. J. S., & Band, G. P. H. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00397 · Cited by 342 · see citing works
Chronic stress and glucocorticoids: From neuronal plasticity to neurodegeneration
Vyas, S., Rodrigues, A. J., Silva, J. M., Tronche, F., Almeida, O. F. X., Sousa, N., & Sotiropoulos, I. (2016) · Neural Plasticity · doi:10.1155/2016/6391686 · Cited by 297 · see citing works
Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications
Yan, Z., & Rein, B. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01092-3 · Cited by 300 · see citing works
Recognizing resilience: Learning from the effects of stress on the brain
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.09.001 · Cited by 292 · see citing works
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Prefrontal Cortex Development in Health and Disease: Lessons from Rodents and Humans
Chini, M., & Hanganu-Opatz, I. L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.017 · Cited by 253 · see citing works
Acute Stress Impairs Self-Control in Goal-Directed Choice by Altering Multiple Functional Connections within the Brain’s Decision Circuits
Maier, S. U., Makwana, A. B., & Hare, T. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.005 · Cited by 270 · see citing works
The neuro-environmental loop of plasticity: a cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving
Callaghan, B. L., & Tottenham, N. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.204 · Cited by 268 · see citing works
The Biology of Human Resilience: Opportunities for Enhancing Resilience Across the Life Span
Feder, A., Fred-Torres, S., Southwick, S. M., & Charney, D. S. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.07.012 · Cited by 269 · see citing works
Spine synapse remodeling in the pathophysiology and treatment of depression
Duman, C. H., & Duman, R. S. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.022 · Cited by 257 · see citing works
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
Hippocampal Sirtuin 1 signaling mediates depression-like behavior
Abe-Higuchi, N., Uchida, S., Yamagata, H., Higuchi, F., Hobara, T., Hara, K., Kobayashi, A., & Watanabe, Y. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.01.009 · Cited by 247 · see citing works
60 YEARS OF NEUROENDOCRINOLOGY: Redefining neuroendocrinology: stress, sex and cognitive and emotional regulation
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0121 · Cited by 253 · see citing works
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Mindfulness, Compassion, and Self-Compassion Among Health Care Professionals: What’s New? A Systematic Review
Conversano, C., Ciacchini, R., Orrù, G., Di Giuseppe, M., Gemignani, A., & Poli, A. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01683 · Cited by 243 · see citing works
“Mindfulness exercises are related to a lower activation of the hypothalamicpituitary-adrenal axis and cortisol secretion, influencing the stress response and its regulation, leading to a greater brain neuroplasticity and slowing the brain aging process (Brewer et al., 2011; Hölzel et al., 2013; McEwen and Morrison, 20…”
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The Brain on Stress: Toward an Integrative Approach to Brain, Body, and Behavior
McEwen, B. S. (2013) · Perspectives on Psychological Science · doi:10.1177/1745691613506907 · Cited by 237 · see citing works
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Reinforcement learning in depression: a review of computational research
Chen, C., Takahashi, T., Nakagawa, S., Inoue, T., & Kusumi, I. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.005 · Cited by 233 · see citing works
Cellular and molecular basis for stress-induced depression
Seo, J.-S., Wei, J., Qin, L., Kim, Y., Yan, Z., & Greengard, P. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.118 · Cited by 235 · see citing works
Duration of early adversity and structural brain development in post-institutionalized adolescents
Hodel, A. S., Hunt, R. H., Cowell, R. A., Van Den Heuvel, S. E., Gunnar, M. R., & Thomas, K. M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.020 · Cited by 220 · see citing works
Psychobiological factors of resilience and depression in late life
Laird, K. T., Krause, B., Funes, C., & Lavretsky, H. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0424-7 · Cited by 229 · see citing works
Allostasis and the Epigenetics of Brain and Body Health Over the Life Course: The Brain on Stress
McEwen, B. S. (2017) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2017.0270 · Cited by 223 · see citing works
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The stressed synapse 2.0: pathophysiological mechanisms in stress-related neuropsychiatric disorders
Sanacora, G., Yan, Z., & Popoli, M. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00540-x · Cited by 197 · see citing works
Mind the gap: glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility
Nasca, C., Bigio, B., Zelli, D., Nicoletti, F., & McEwen, B. S. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.96 · Cited by 194 · see citing works
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Neuroanatomical Correlates of the Income-Achievement Gap
Mackey, A. P., Finn, A. S., Leonard, J. A., Jacoby-Senghor, D. S., West, M. R., Gabrieli, C. F. O., & Gabrieli, J. D. E. (2015) · Psychological Science · doi:10.1177/0956797615572233 · Cited by 176 · see citing works
Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner
Zhang, J.-Y., Liu, T.-H., He, Y., Pan, H.-Q., Zhang, W.-H., Yin, X.-P., Tian, X.-L., Li, B.-M., Wang, X.-D., Holmes, A., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.019 · Cited by 183 · see citing works
Peripheral and central mechanisms of stress resilience
Pfau, M. L., & Russo, S. J. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.09.004 · Cited by 170 · see citing works
Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction
Bhattacherjee, A., Djekidel, M. N., Chen, R., Chen, W., Tuesta, L. M., & Zhang, Y. (2019) · Nature Communications · doi:10.1038/s41467-019-12054-3 · Cited by 174 · see citing works
Does the brain shrink as the waist expands?
Willette, A. A., & Kapogiannis, D. (2015) · Ageing Research Reviews · doi:10.1016/j.arr.2014.03.007 · Cited by 162 · see citing works
GABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response
Gunn, B. G., Cunningham, L., Mitchell, S. G., Swinny, J. D., Lambert, J. J., & Belelli, D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.06.001 · Cited by 149 · see citing works
Synaptic Loss and the Pathophysiology of PTSD: Implications for Ketamine as a Prototype Novel Therapeutic
Krystal, J. H., Abdallah, C. G., Averill, L. A., Kelmendi, B., Harpaz-Rotem, I., Sanacora, G., Southwick, S. M., & Duman, R. S. (2017) · Current Psychiatry Reports · doi:10.1007/s11920-017-0829-z · Cited by 145 · see citing works
Protective Prevention Effects on the Association of Poverty With Brain Development
Brody, G. H., Gray, J. C., Yu, T., Barton, A. W., Beach, S. R. H., Galván, A., MacKillop, J., Windle, M., Chen, E., Miller, G. E., et al. (2017) · JAMA Pediatrics · doi:10.1001/jamapediatrics.2016.2988 · Cited by 135 · see citing works
Efficacy of Mindfulness-Based Cognitive Training in Surgery: Additional Analysis of the Mindful Surgeon Pilot Randomized Clinical Trial
Lebares, C. C., Guvva, E. V., Olaru, M., Sugrue, L. P., Staffaroni, A. M., Delucchi, K. L., Kramer, J. H., Ascher, N. L., & Harris, H. W. (2019) · JAMA Network Open · doi:10.1001/jamanetworkopen.2019.4108 · Cited by 131 · see citing works
Altered amygdala connectivity in urban youth exposed to trauma
Thomason, M. E., Marusak, H. A., Tocco, M. A., Vila, A. M., McGarragle, O., & Rosenberg, D. R. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv030 · Cited by 127 · see citing works
“Animals that experience early life adversity show structural and functional changes in both the amygdala (Malter Cohen et al., 2013b for a review) and PFC (review by McEwen and Morrison, 2013).”
Background
Peripheral Elevation of a Klotho Fragment Enhances Brain Function and Resilience in Young, Aging, and α-Synuclein Transgenic Mice
Leon, J., Moreno, A. J., Garay, B. I., Chalkley, R. J., Burlingame, A. L., Wang, D., & Dubal, D. B. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.024 · Cited by 123 · see citing works
Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than in males
Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.02.023 · Cited by 125 · see citing works
A POMC-originated circuit regulates stress-induced hypophagia, depression, and anhedonia
Qu, N., He, Y., Wang, C., Xu, P., Yang, Y., Cai, X., Liu, H., Yu, K., Pei, Z., Hyseni, I., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0506-1 · Cited by 122 · see citing works
Stress-induced mechanisms in mental illness: A role for glucocorticoid signalling
Cattaneo, A., & Riva, M. A. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.07.021 · Cited by 118 · see citing works
Linking inflammation, aberrant glutamate-dopamine interaction, and post-synaptic changes: translational relevance for schizophrenia and antipsychotic treatment: a systematic review
de Bartolomeis, A., Barone, A., Vellucci, L., Mazza, B., Austin, M. C., Iasevoli, F., & Ciccarelli, M. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02976-3 · Cited by 113 · see citing works
Role of the Astroglial Glutamate Exchanger xCT in Ventral Hippocampus in Resilience to Stress
Nasca, C., Bigio, B., Zelli, D., de Angelis, P., Lau, T., Okamoto, M., Soya, H., Ni, J., Brichta, L., Greengard, P., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.020 · Cited by 113 · see citing works
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Complement component 3a receptor deficiency attenuates chronic stress-induced monocyte infiltration and depressive-like behavior
Crider, A., Feng, T., Pandya, C. D., Davis, T., Nair, A., Ahmed, A. O., Baban, B., Turecki, G., & Pillai, A. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.03.004 · Cited by 112 · see citing works
Cognitive Dysfunction in Depression – Pathophysiology and Novel Targets
Carvalho, A., Miskowiak, K., Hyphantis, T., Kohler, C., Alves, G., Bortolato, B., G. Sales, P., Machado-Vieira, R., Berk, M., & McIntyre, R. (2015) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527313666141130203627 · Cited by 107 · see citing works
Stress-induced remodeling of hippocampal CA3 pyramidal neurons
McEwen, B. S. (2016) · Brain Research · doi:10.1016/j.brainres.2015.12.043 · Cited by 105 · see citing works
Self-citation
Stress during a critical postnatal period induces region-specific structural abnormalities and dysfunction of the prefrontal cortex via CRF1
Yang, X.-D., Liao, X.-M., Uribe-Mariño, A., Liu, R., Xie, X.-M., Jia, J., Su, Y.-A., Li, J.-T., Schmidt, M. V., Wang, X.-D., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.304 · Cited by 93 · see citing works
Future directions in the study of early-life stress and physical and emotional health: implications of the neuroimmune network hypothesis.
Hostinar, C. E., Nusslock, R., & Miller, G. E. (2018) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2016.1266647 · Cited by 90 · see citing works
Functional and Structural Remodeling of Glutamate Synapses in Prefrontal and Frontal Cortex Induced by Behavioral Stress
Musazzi, L., Treccani, G., & Popoli, M. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00060 · Cited by 83 · see citing works
Early secure attachment as a protective factor against later cognitive decline and dementia
Walsh, E., Blake, Y., Donati, A., Stoop, R., & von Gunten, A. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00161 · Cited by 84 · see citing works
Adolescent nicotine exposure induces dysregulation of mesocorticolimbic activity states and depressive and anxiety-like prefrontal cortical molecular phenotypes persisting into adulthood
Jobson, C. L. M., Renard, J., Szkudlarek, H., Rosen, L. G., Pereira, B., Wright, D. J., Rushlow, W., & Laviolette, S. R. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy179 · Cited by 64 · see citing works
Long-range orbitofrontal and amygdala axons show divergent patterns of maturation in the frontal cortex across adolescence
Johnson, C. M., Loucks, F. A., Peckler, H., Thomas, A. W., Janak, P. H., & Wilbrecht, L. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.01.005 · Cited by 59 · see citing works
The Selective RhoA Inhibitor Rhosin Promotes Stress Resiliency Through Enhancing D1-Medium Spiny Neuron Plasticity and Reducing Hyperexcitability
Francis, T. C., Gaynor, A., Chandra, R., Fox, M. E., & Lobo, M. K. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.02.007 · Cited by 61 · see citing works
Lost in translation: How to upgrade fear memory research
Flores, Á., Fullana, M. À., Soriano-Mas, C., & Andero, R. (2018) · Molecular Psychiatry · doi:10.1038/s41380-017-0006-0 · Cited by 59 · see citing works
Histone Modification ofNedd4Ubiquitin Ligase Controls the Loss of AMPA Receptors and Cognitive Impairment Induced by Repeated Stress
Wei, J., Xiong, Z., Lee, J. B., Cheng, J., Duffney, L. J., Matas, E., & Yan, Z. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3056-15.2016 · Cited by 56 · see citing works
Neurobiology of the rapid-acting antidepressant effects of ketamine: impact and opportunities
Shinohara, R., Aghajanian, G. K., & Abdallah, C. G. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.12.006 · Cited by 54 · see citing works
The dose makes the poison: From glutamate-mediated neurogenesis to neuronal atrophy and depression
Rubio-Casillas, A., & Fernández-Guasti, A. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0066 · Cited by 49 · see citing works
Differential effect of COMT gene methylation on the prefrontal connectivity in subjects with depression versus healthy subjects
Na, K.-S., Won, E., Kang, J., Kim, A., Choi, S., Tae, W.-S., Kim, Y.-K., Lee, M.-S., Joe, S.-H., & Ham, B.-J. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.030 · Cited by 50 · see citing works
Antidepressant administration modulates stress-induced DNA methylation and DNA methyltransferase expression in rat prefrontal cortex and hippocampus
Sales, A. J., & Joca, S. R. L. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.01.022 · Cited by 47 · see citing works
Coping with Stress During Aging: The Importance of a Resilient Brain
Sampedro-Piquero, P., Alvarez-Suarez, P., & Begega, A. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666170915141610 · Cited by 41 · see citing works
Juvenile stress induces behavioral change and affects perineuronal net formation in juvenile mice
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., Aoki, S., & Ishihara, T. (2018) · BMC Neuroscience · doi:10.1186/s12868-018-0442-z · Cited by 39 · see citing works
Chronic stress-induced neuroplasticity in the prefrontal cortex: Structural, functional, and molecular mechanisms from development to aging
Algaidi, S. A. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149461 · Cited by 40 · see citing works
Brain-derived neurotrophic factor DNA methylation mediates the association between neighborhood disadvantage and adolescent brain structure
Wrigglesworth, J., Ryan, J., Vijayakumar, N., & Whittle, S. (2019) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2018.12.012 · Cited by 34 · see citing works
Developmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
“…behavior through its roles in suppressing aggression, monitoring approach/avoid conflict, and modulating the stress response via its projections to the MeA and other stress-modulatory nodes (Aupperle & Paulus, 2010; McEwen & Morrison, 2013; Takahashi, Nagayasu, Nishitani, Kaneko, & Koide, 2014).”
Background
Chronic Desipramine Prevents Acute Stress-Induced Reorganization of Medial Prefrontal Cortex Architecture by Blocking Glutamate Vesicle Accumulation and Excitatory Synapse Increase
Nava, N., Treccani, G., Liebenberg, N., Chen, F., Popoli, M., Wegener, G., & Nyengaard, J. R. (2015) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu085 · Cited by 32 · see citing works
Early emergence of altered 5‐HT2Areceptor‐evoked behavior, neural activation and gene expression following maternal separation
Sood, A., Pati, S., Bhattacharya, A., Chaudhari, K., & Vaidya, V. A. (2018) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.10.005 · Cited by 25 · see citing works
Neuroimmune modulation of pain across the developmental spectrum
Karshikoff, B., Tadros, M. A., Mackey, S., & Zouikr, I. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.01.010 · Cited by 21 · see citing works
What Does CATS Have to Do With Cancer? The Cognitive Activation Theory of Stress (CATS) Forms the SURGE Model of Chronic Post-surgical Pain in Women With Breast Cancer.
Munk, A., Reme, S. E., & Jacobsen, H. B. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.630422 · Cited by 16 · see citing works
Genome to Phenome: A Systems Biology Approach to PTSD Using an Animal Model
Chakraborty, N., Meyerhoff, J., Jett, M., & Hammamieh, R. (2017) · Methods in Molecular Biology · doi:10.1007/978-1-4939-6952-4_6 · Cited by 14 · see citing works
Abnormal brain gray matter volume in patients with major depressive disorder: Associated with childhood trauma?
Liu, Y., Zhang, J., Zhang, M., Li, X., Li, K., Wang, B., Yang, Y., Song, R., Si, Y., Ni, T., et al. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.04.083 · Cited by 14 · see citing works
Primary ciliary protein kinase A activity in the prefrontal cortex modulates stress in mice
Yang, J., Dong, Y., Liu, J., Peng, Y., Wang, D., Li, L., Hu, X., Li, J., Wang, L., Chu, J., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.02.002 · Cited by 10 · see citing works
The clinical use of epigenetics in psychiatry: a narrative review of epigenetic mechanisms, key candidate genes, and precision psychiatry
Montel Hayes, R., Mason, C. E., & Miller, J. J. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1671122 · Cited by 5 · see citing works
Emotionally based strategic communications as a new tool in defensive cognitive warfare
Ćosić, K., Popović, S., & Wiederhold, B. (2026) · Frontiers in Psychology · doi:10.3389/fpsyg.2026.1751406 · Cited by 4 · see citing works
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Authors: McEwen, B. S., & Morrison, J. H.
Affiliations: Rockefeller University (US)
Icahn School of Medicine at Mount Sinai (US)
Corresponding author: McEwen, Bruce S.
ORCID: McEwen, Bruce S.
Morrison, John H.
Venue: Neuron
Publisher: Elsevier BV
Published: 2013-07
Volume: 79
Issue: 1
Pages: 16-29
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2013.06.028
PMC: PMC3753223
OpenAlex: W2102178526
Cited by: 1,079
References: 162
Citations by year: 2026: 120 · 2025: 98 · 2024: 67 · 2023: 62 · 2022: 73 · 2021: 105 · 2020: 98 · 2019: 71 · 2018: 105 · 2017: 77 · 2016: 71 · 2015: 79 · 2014: 46 · 2013: 4
FWCI: 5.49
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 374 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (P01AG016765)
National Institute of Mental Health (R01MH041256)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: prefrontal cortex, stress, neuroplasticity, life course, neuronal resilience, neuroendocrine function, autonomic function, infancy, adolescence, aging, sex differences, sex hormones, self-regulation, working memory
MeSH terms: Cognition, Humans, Life Change Events, Memory, Short-Term, Neuronal Plasticity, Stress, Psychological, Prefrontal Cortex

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The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course

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