Stress, memory and the amygdala

Benno Roozendaal; Bruce S. McEwen; Sumantra Chattarji

doi:10.1038/nrn2651

journal article May 13, 2009

Stress, memory and the amygdala

Benno Roozendaal Bruce S. McEwen Sumantra Chattarji

Nature Reviews Neuroscience Vol. 10 No. 6 pp. 423-433 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/nrn2651

Topics

No keywords indexed for this article. Browse by subject →

References

132

[1]

Stress, Adaptation, and Disease: Allostasis and Allostatic Load

Bruce S. McEwen

Annals of the New York Academy of Sciences 1998 10.1111/j.1749-6632.1998.tb09546.x

[2]

Neisser, U. et al. Remembering the earthquake: direct experience vs. hearing the news. Memory 4, 337–357 (1996). 10.1080/096582196388898

[3]

Bohannon, J. N. Flashbulb memories for the space shuttle disaster: a tale of two theories. Cognition 29, 179–196 (1988). 10.1016/0010-0277(88)90036-4

[4]

Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5

R. G. M. Morris, E. Anderson, G. S. Lynch et al.

Nature 1986 10.1038/319774a0

[5]

Vazdarjanova, A. & McGaugh, J. L. Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning. Proc. Natl Acad. Sci. USA 95, 15003–15007 (1998). 10.1073/pnas.95.25.15003

[6]

McGaugh, J. L. & Roozendaal, B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr. Opin. Neurobiol. 12, 205–210 (2002). 10.1016/s0959-4388(02)00306-9

[7]

McEwen, B. S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873–904 (2007). 10.1152/physrev.00041.2006

[8]

Sheline, Y. I. Neuroimaging studies of mood disorder effects on the brain. Biol. Psychiatry 54, 338–352 (2003). 10.1016/s0006-3223(03)00347-0

[9]

Joels, M. & Baram, T. Z. The neuro-symphony of stress. Nature Rev. Neurosci. 2 Apr 2009 (doi:10.1038/nrn2632). These authors report why stress requires the activation of many different stress mediators and how the effects of individual mediators on neuronal function and plasticity are integrated. 10.1038/nrn2632

[10]

McGaugh, J. L. Memory--a century of consolidation. Science 287, 248–251 (2000). A comprehensive review of memory consolidation research, focusing on the role of the amygdala, and the noradrenergic system in the BLA, in modulating long-term memory consolidation in other brain regions. 10.1126/science.287.5451.248

[11]

Galvez, R., Mesches, M. H. & McGaugh, J. L. Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiol. Learn. Mem. 66, 253–257 (1996). 10.1006/nlme.1996.0067

[12]

Hatfield, T. & McGaugh, J. L. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol. Learn. Mem. 71, 232–239 (1999). 10.1006/nlme.1998.3875

[13]

Liang, K. C., McGaugh, J. L. & Yao, H. Y. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 508, 225–233 (1990). 10.1016/0006-8993(90)90400-6

[14]

Ferry, B., Roozendaal, B. & McGaugh, J. L. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between β- and α1-adrenoceptors. J. Neurosci. 19, 5119–5123 (1999). 10.1523/jneurosci.19-12-05119.1999

[15]

Ferry, B., Roozendaal, B. & McGaugh, J. L. Involvement of α1-adrenoceptors in the basolateral amygdala in modulation of memory storage. Eur. J. Pharmacol. 372, 9–16 (1999). 10.1016/s0014-2999(99)00169-7

[16]

Brioni, J. D., Nagahara, A. H. & McGaugh, J. L. Involvement of the amygdala GABAergic system in the modulation of memory storage. Brain Res. 487, 105–112 (1989). 10.1016/0006-8993(89)90945-1

[17]

Wilensky, A. E., Schafe, G. E. & LeDoux, J. E. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. J. Neurosci. 20, 7059–7066 (2000). 10.1523/jneurosci.20-18-07059.2000

[18]

Marsicano, G. et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530–534 (2002). 10.1038/nature00839

[19]

Campolongo, P. et al. Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc. Natl Acad. Sci. USA 106, 4888–4893 (2009). These authors show that activation of endocannabinoid CB1 activity in the BLA enhances memory consolidation and provide the first in vivo demonstration in mammals that endocannabinoid activity is required to enable the memory-enhancing effects of glucocorticoids. 10.1073/pnas.0900835106

[20]

Katona, I. et al. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19, 4544–4558 (1999). 10.1523/jneurosci.19-11-04544.1999

[21]

Hoffman, A. F. & Lupica, C. R. Mechanisms of cannabinoid inhibition of GABAA synaptic transmission in the hippocampus. J. Neurosci. 20, 2470–2479 (2000). 10.1523/jneurosci.20-07-02470.2000

[22]

Williams, C. L., Men, D., Clayton, E. C. & Gold, P. E. Norepinephrine release in the amygdala after systemic injection of epinephrine or escapable footshock: contribution of the nucleus of the solitary tract. Behav. Neurosci. 112, 1414–1422 (1998). 10.1037/0735-7044.112.6.1414

[23]

Liang, K. C., Juler, R. G. & McGaugh, J. L. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res. 368, 125–133 (1986). 10.1016/0006-8993(86)91049-8

[24]

McGaugh, J. L., Cahill, L. & Roozendaal, B. Involvement of the amygdala in memory storage: interaction with other brain systems. Proc. Natl Acad. Sci. USA 93, 13508–13514 (1996). 10.1073/pnas.93.24.13508

[25]

Clayton, E. C. & Williams, C. L. Adrenergic activation of the nucleus tractus solitarius potentiates amygdala norepinephrine release and enhances retention performance in emotionally arousing and spatial memory tasks. Behav. Brain Res. 112, 151–158 (2000). These authors reported evidence that adrenaline infused into the nucleus of the solitary tract enhances retention of inhibitory avoidance and radial-maze spatial training. In addition, the adrenaline infusions potentiated noradrenaline release in the amygdala, as assessed by in vivo microdialysis and high-performance liquid chromatography. 10.1016/s0166-4328(00)00178-9

[26]

Williams, C. L. & Clayton, E. C. in Memory Consolidation: Essays in Honor of James L. McGaugh (eds Gold, P. E. & Greenough, W. T.) 141–163 (American Psychological Association, Washington DC, 2001). 10.1037/10413-008

[27]

Fallon, J. H. & Ciofi, P. in The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.) 97–114 (Wiley-Liss, New York, 1992).

[28]

Reul, J. M. & de Kloet, E. R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117, 2505–2511 (1985). 10.1210/endo-117-6-2505

[29]

Roozendaal, B. & McGaugh, J. L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol. Learn. Mem. 67, 176–179 (1997). 10.1006/nlme.1996.3765

[30]

Donley, M. P., Schulkin, J. & Rosen, J. B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behav. Brain Res. 164, 197–205 (2005). 10.1016/j.bbr.2005.06.020

[31]

Roozendaal, B. & McGaugh, J. L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem. 65, 1–8 (1996). 10.1006/nlme.1996.0001

[32]

Roozendaal, B., Portillo-Marquez, G. & McGaugh, J. L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav. Neurosci. 110, 1074–1083 (1996). 10.1037/0735-7044.110.5.1074

[33]

Quirarte, G. L., Roozendaal, B. & McGaugh, J. L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl Acad. Sci. USA 94, 14048–14053 (1997). 10.1073/pnas.94.25.14048

[34]

Roozendaal, B., Quirarte, G. L. & McGaugh, J. L. Glucocorticoids interact with the basolateral amygdala β-adrenoceptor–cAMP/cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. 15, 553–560 (2002). 10.1046/j.0953-816x.2001.01876.x

[35]

Roozendaal, B., Schelling, G. & McGaugh, J. L. Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the β-adrenoceptor-cAMP pathway: dependence on glucocorticoid receptor activation. J. Neurosci. 28, 6642–6651 (2008). 10.1523/jneurosci.1336-08.2008

[36]

Buchanan, T. W. & Lovallo, W. R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26, 307–317 (2001). 10.1016/s0306-4530(00)00058-5

[37]

Cahill, L. et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Natl Acad. Sci. USA 93, 8016–8021 (1996). 10.1073/pnas.93.15.8016

[38]

Cahill, L. & Alkire, M. T. Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiol. Learn. Mem. 79, 194–198 (2003). 10.1016/s1074-7427(02)00036-9

[39]

Okuda, S., Roozendaal, B. & McGaugh, J. L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc. Natl Acad. Sci. USA 101, 853–858 (2004). 10.1073/pnas.0307803100

[40]

Roozendaal, B., Okuda, S., Van der Zee, E. A. & McGaugh, J. L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl Acad. Sci. USA 103, 6741–6746 (2006). 10.1073/pnas.0601874103

[41]

Roozendaal, B., Okuda, S., Van der Zee, E. A. & McGaugh, J. L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl Acad. Sci. USA 103, 6741–6746 (2006). This study showed that glucocorticoids require emotional arousal-induced noradrenergic activation in the BLA to influence memory consolidation. 10.1073/pnas.0601874103

[42]

Cahill, L., Prins, B., Weber, M. & McGaugh, J. L. β-Adrenergic activation and memory for emotional events. Nature 371, 702–704 (1994). 10.1038/371702a0

[43]

Nielson, K. A. & Jensen, R. A. Beta-adrenergic receptor antagonist antihypertensive medications impair arousal-induced modulation of working memory in elderly humans. Behav. Neural Biol. 62, 190–200 (1994). 10.1016/s0163-1047(05)80017-2

[44]

Cahill, L., Babinsky, R., Markowitsch, H. J. & McGaugh, J. L. The amygdala and emotional memory. Nature 377, 295–296 (1995). 10.1038/377295a0

[45]

Pikkarainen, M., Ronkko, S., Savander, V., Insausti, R. & Pitkanen, A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 403, 229–260 (1999). 10.1002/(sici)1096-9861(19990111)403:2<229::aid-cne7>3.0.co;2-p

[46]

Petrovich, G. D., Canteras, N. S. & Swanson, L. W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 38, 247–289 (2001). 10.1016/s0165-0173(01)00080-7

[47]

McDonald, R. J. & White, N. M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav. Neurosci. 107, 3–22 (1993). 10.1037/0735-7044.107.1.3

[48]

Packard, M. G. & McGaugh, J. L. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 106, 439–446 (1992). 10.1037/0735-7044.106.3.439

[49]

Packard, M. G., Cahill, L. & McGaugh, J. L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl Acad. Sci. USA 91, 8477–8481 (1994). 10.1073/pnas.91.18.8477

[50]

McIntyre, C. K. et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc. Natl Acad. Sci. USA 102, 10718–10723 (2005). 10.1073/pnas.0504436102

Showing 50 of 132 references

Cited By

1,448

Transcriptomic reprogramming of the medial amygdala in chronic stress: Implications of ER proteostasis and neuropeptide signaling for anxiety-like behaviors

Shengru Hu, Zixu Zhang · 2026

Journal of Affective Disorders

Transcriptomic profiles of susceptibility and resilience to stress in the amygdala and hippocampus of male rats

Kimberly L.P. Long, Sandra E. Muroy · 2025

Neurobiology of Stress

The Relationship Between Brain Activation for Taking Others’ Perspective and Interoceptive Abilities in Autism Spectrum Disorder: An fMRI Study

Huiyeong Jeon, Ahjeong Hur · 2024

Journal of the Korean Academy of Ch...

Basolateral amygdala parvalbumin and cholecystokinin-expressing GABAergic neurons modulate depressive and anxiety-like behaviors

Muhammad Asim, Huajie Wang · 2024

Translational Psychiatry

Transcriptome dynamics in mouse amygdala under acute and chronic stress revealed by thiol-labeled RNA sequencing

Dan Zhao, Lu Zhang · 2024

Neurobiology of Stress

Cholecystokinin B receptor antagonists for the treatment of depression via blocking long-term potentiation in the basolateral amygdala

Xu Zhang, Muhammad Asim · 2023

Molecular Psychiatry

Association between adverse childhood experiences and brain volumes among Japanese community-dwelling older people: Findings from the NEIGE study

Yuna Koyama, Takeo Fujiwara · 2022

Child Abuse & Neglect

Increased Anxiety-like Behaviors in Adgra1−/− Male But Not Female Mice are Attributable to Elevated Neuron Dendrite Density, Upregulated PSD95 Expression, and Abnormal Activation of the PI3K/AKT/GSK-3β and MEK/ERK Pathways

Xiao-Hong Zhang, Chun-Ling Shen · 2022

Neuroscience

Functional brain‐wide network mapping during acute stress exposure in rats: Interaction between the lateral habenula and cortical, amygdalar, hypothalamic and monoaminergic regions

Laura Durieux, Karine Herbeaux · 2022

European Journal of Neuroscience

Juvenile exposure to acute traumatic stress leads to long-lasting alterations in grey matter myelination in adult female but not male rats

Jocelyn M. Breton, Matthew Barraza · 2021

Neurobiology of Stress

Agreement Between Prospective and Retrospective Measures of Childhood Maltreatment

Jessie R. Baldwin, Aaron Reuben · 2019

JAMA Psychiatry

Interactive effects of stress reactivity and rapid eye movement sleep theta activity on emotional memory formation

Sara Y. Kim, Sarah M. Kark · 2019

Hippocampus

Chronic social defeat stress induces sustained synaptic structural changes in the prefrontal cortex and amygdala

L. Colyn, E. Venzala · 2019

Behavioural Brain Research

Dopamine System Dysregulation in Major Depressive Disorders

Pauline Belujon, Anthony A Grace · 2017

The International Journal of Neurop...

How do antidepressants work? New perspectives for refining future treatment approaches

Catherine J Harmer, Ronald S Duman · 2017

The Lancet Psychiatry

NEVER forget: negative emotional valence enhances recapitulation

Holly J. Bowen, Sarah M. Kark · 2017

Psychonomic Bulletin & Review

Mediodorsal nucleus and its multiple cognitive functions

Erin C. Golden, Jonathan Graff-Radford · 2016

Neurology

The impact of chronic stress on the rat brain lipidome

T G Oliveira, R B Chan · 2015

Molecular Psychiatry

Memory reconsolidation, emotional arousal, and the process of change in psychotherapy: New insights from brain science

RICHARD D. LANE, Lee Ryan · 2014

Behavioral and Brain Sciences

Distinct structural plasticity in the hippocampus and amygdala of the middle-aged common marmoset (Callithrix jacchus)

Michael W. Marlatt, Ingrid Philippens · 2011

Experimental Neurology

Metrics

1,448

Citations

132

References

Details

Published: May 13, 2009
Vol/Issue: 10(6)
Pages: 423-433
License: View

Authors

Fishberg Department of Neuroscience and Kastor Neurobiology of Aging Laboratories, Friedman Brain Institute, Department of Geriatrics and Palliative Medicine, Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, New York; and Harold and Margaret Milliken Hatch Laboratory of Neuroendocrinology, The Rockefeller University, New York, New York

S

Sumantra Chattarji

Cite This Article

Benno Roozendaal, Bruce S. McEwen, Sumantra Chattarji (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10(6), 423-433. https://doi.org/10.1038/nrn2651

Stress, memory and the amygdala

You May Also Like