Cited by 301Memory and Neural MechanismsMemory Processes and InfluencesStress Responses and Cortisol

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Modulation of memory storage

Cahill, Larry, McGaugh, James L·1996·Current Opinion in Neurobiology

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Abstract

For several decades, the concept of modulation of memory storage has significantly influenced research investigating neurobiological memory mechanisms. New evidence provides additional support for the view that stress hormones released during emotionally arousing situations modulate memory processes. Recent experiments have investigated the role of sympathetic adrenomedullary hormones in emotional memory in humans, as well as the role of adrenocortical hormones, primarily in animal studies. Further, it is becoming increasingly clear that the sympathetic adrenomedullary and the pituitary adrenocortical systems interact to modulate memory storage. Other new evidence emphasizes the role of peripheral influences to the brain on emotional memory, as well as the critical contribution of the amygdaloid complex in modulation of memory by emotional arousal.

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Retracted
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“Learning depends on the emotional context in which it occurs [Cahill and McGaugh, 1996].”
Background
Individual differences in factors that modulate storage and retrieval of traumatic memories
Howe, M. L. (1998) · Development and Psychopathology · doi:10.1017/s0954579498001813 · Cited by 27
“As Cahill and McGaugh (1996) point out, theby which memory is transformed from a labile, transient form to a more stable, less vola- role of glucose in the modulation of memory storage may be specific to the learning situa-tile form.”
Background
Associations between endogenous cortisol levels and emotional memory in young women: Influence of encoding instructions
Preuss, D., Schoofs, D., & Wolf, O. T. (2009) · Stress · doi:10.1080/10253890802524592 · Cited by 26
(±)-α-Methyl-4-carboxyphenylglycine, a metabotropic glutamate receptor blocker, impairs retention of an inhibitory avoidance task in rats when infused into the basolateral nucleus of the amygdala
Bianchin, M. M., Spanis, C. W., Roesler, R., McGaugh, J. L., & Izquierdo, I. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02220-9 · Cited by 24
Self-citation
The origins of effortful control: How early development within arousal/regulatory systems influences attentional and affective control
Wass, S. V. (2021) · Developmental Review · doi:10.1016/j.dr.2021.100978 · Cited by 36
Chronic administration of propranolol impairs inhibitory avoidance retention in mice.
Nielson, K. A., Czech, D. A., & Laubmeier, K. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3873 · Cited by 25
“Emotional and physiological arousal are believed to play important mediating roles in the enhancement or impairment of memory storage processes by making important stimuli stand apart from those that are minor or insignificant (Cahill & McGaugh, 1996).”
Background
Molecular brake pad hypothesis: pulling off the brakes for emotional memory
Vogel-Ciernia, A., & Wood, M. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0050 · Cited by 25
“Emotionally arousing experiences tend to be better remembered and these memories can last for the lifetime of the organism (reviewed in Cahill and McGaugh, 1996; McGaugh, 2000, 2004).”
Background
Japanese Quail’s Genetic Background Modulates Effects of Chronic Stress on Emotional Reactivity but Not Spatial Learning
Laurence, A., Houdelier, C., Petton, C., Calandreau, L., Arnould, C., Favreau-Peigné, A., Leterrier, C., Boissy, A., Richard‐Yris, M., & Lumineau, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047475 · Cited by 27
“However, to modulate the memory system these emotions have to occur close enough in time to the learning task [74,82].”
Background
Persistent frontal P300 brain potential suggests abnormal processing of auditory information in distractible children.
Kilpeläinen, R., Luoma, L., Herrgård, E., Yppärilä, H., Partanen, J., & Karhu, J. (1999) · NeuroReport · doi:10.1097/00001756-199911080-00027 · Cited by 24
Memory and Developmental Psychopathology
Howe, M. L., Toth, S. L., & Cicchetti, D. (2015) · Wiley eBooks · doi:10.1002/9780470939390.ch15 · Cited by 33
Untitled work
McEwen (2004) · doi:10.1016/s1054-3589(04)50016-9 · Cited by 22
Memory-enhancing treatments reverse the impairment of inhibitory avoidance retention in sepsis-surviving rats
Tuon, L., Comim, C. M., Petronilho, F. C., Barichello, T., Izquierdo, I., Quevedo, J., & Dal‐Pizzol, F. (2008) · Critical Care · doi:10.1186/cc7103 · Cited by 20
“For example, opioid receptors are involved in memory modulation, and post-training injections of the opioid antagonist naloxone (NAL) enhance retention of inhibitory avoidance in rats [9].”
Background
Agents that affect cAMP levels or protein kinase A activity modulate memory consolidation when injected into rat hippocampus but not amygdala.
Bevilaqua, L., Ardenghi, P., Schröder, N., Bromberg, E., Quevedo, J., Schmitz, P., Bianchin, M., Walz, R., Schaeffer, E., Medina, J., et al. (1997) · Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas · doi:10.1590/s0100-879x1997000800009 · Cited by 22
“The first one was at 0 h after training and coincided with the early labile phase of memory (7).”
Background
New meanings of thin-skinned: The contrasting attentional profiles of typical 12-month-olds who show high, and low, stress reactivity.
Wass, S. V., de Barbaro, K., Clackson, K., & Leong, V. (2018) · Developmental Psychology · doi:10.1037/dev0000428 · Cited by 13
β-adrenergic receptors reduce the threshold for induction and stabilization of LTP and enhance its magnitude via multiple mechanisms in the ventral but not the dorsal hippocampus
Papaleonidopoulos, V., & Papatheodoropoulos, C. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.010 · Cited by 18
“…Riekkinen, & Feenstra, 1999; Kocsis, Li, & Hajos, 2007) facilitating the induction of synaptic modifications (Hu et al., 2007; O'Dell et al., 2015) and the establishment of memory of emotionally charged events (Cahill & McGaugh, 1996; Kukolja, Klingmuller, Maier, Fink, & Hurlemann, 2011).”
The effects of affect and input source on flashbulb memories
Bohannon, J., Gratz, S., & Cross, V. (2007) · Applied Cognitive Psychology · doi:10.1002/acp.1372 · Cited by 20
The Role of Sleep in Memory Consolidation
Payne, J. D., Ellenbogen, J. M., Walker, M. P., & Stickgold, R. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00181-9 · Cited by 33
Learning to learn from positive experiences
Hanson, R., Shapiro, S. L., Hutton-Thamm, E., Hagerty, M. R., & Sullivan, K. P. (2021) · The Journal of Positive Psychology · doi:10.1080/17439760.2021.2006759 · Cited by 24
“Increased activity at these receptor sites related to physically-or emotionally-based arousal heightens the formation of explicit and implicit memory (Cahill & McGaugh, 1996).”
Reduction of glutamate release probability and the number of releasable vesicles are required for suppression of glutamatergic transmission by β1-adrenoceptors in the medial prefrontal cortex
Luo, F., Guo, N.-N., Li, S., Tang, H., Liu, Y., & Zhang, Y. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.03.020 · Cited by 22
Positive impact of levetiracetam on emotional learning and memory in naive mice.
Celikyurt, I., Ulak, G., Mutlu, O., Akar, F., Mulayim, S., Erden, F., & Komşuoğlu, S. (2012) · Life Science · doi:10.1016/j.lfs.2011.11.003 · Cited by 19
The growth hormone axis and cognition: empirical results and integrated theory derived from giant transgenic mice
Rollo, C. D., Ko, C. V., Tyerman, J. A., & Kajiura, L. J. (1999) · Canadian Journal of Zoology · doi:10.1139/z99-153 · Cited by 19
“Shortfalls impair neuronal function and induce neurodegeneration (Tucek 1985; Beal 1992; Gold 1992; Stone et al. 1995; Cahill and McGaugh 1996).”
BackgroundInfluential
Enhanced learning by posttrial injection of H1-but not H2-histaminergic antagonists into the nucleus basalis magnocellularis region.
Privou, C., Li, J.-S., Hasenöhrl, R., & Huston, J. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3885 · Cited by 19
The use of the Emotional-Object Recognition as an assay to assess learning and memory associated to an aversive stimulus in rodents
Brancato, A., Lavanco, G., Cavallaro, A., Plescia, F., & Cannizzaro, C. (2016) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2016.09.010 · Cited by 19
Flavour-specific anticipatory hunger reinforced by either carbohydrate or protein.
Thibault, L., & Booth, D. (2006) · Physiology and Behavior · doi:10.1016/j.physbeh.2006.02.007 · Cited by 18
NMDAR Neurotransmission Needed for Persistent Neuronal Firing: Potential Roles in Mental Disorders
Yang, S., Seo, H., Wang, M., & Arnsten, A. F. T. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.654322 · Cited by 17
Influences of protein to energy ratios in breakfast on mood, alertness and attention in the healthy undergraduate students
Zeng, Y.-C., Li, S.-M., Xiong, G.-L., Su, H., & Wan, J.-C. (2011) · Health · doi:10.4236/health.2011.36065 · Cited by 20
“An ‘inverted U’-shaped dose-response curve was reported for the effects of plasma glucose [35], and insulin concentration [36] on cognitive functions.”
Background
Media and Stress in Adolescent Boys in Germany
Maass, A., Lohaus, A., & Wolf, O. T. (2010) · Journal of Children and Media · doi:10.1080/17482790903407259 · Cited by 17
“The release of stress-related hormones and neurotransmitters improves the learning of emotional materials, but, conversely, impairs memory consolidation of neutral learning materials, working memory and memory retrieval (Cahill & McGaugh, 1996 ; Roozendaal, Okuda, de Quervain, & McGaugh, 2006 ; Wolf, 2008 ).”
Background
Vagus nerve stimulation promotes extinction generalization across sensory modalities
de Souza, R. R., Oleksiak, C. R., Tabet, M. N., Rennaker, R. L., Hays, S. A., Kilgard, M. P., & McIntyre, C. K. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107425 · Cited by 15
Emotional Encoding Context Leads to Memory Bias in Individuals with High Anxiety
Lee, C., & Fernandes, M. A. (2017) · Brain Sciences · doi:10.3390/brainsci8010006 · Cited by 16
Angiotensin modulates long-term memory expression but not long-term memory storage in the crab Chasmagnathus
Frenkel, L., Suárez, L. D., Maldonado, H., & Delorenzi, A. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.09.003 · Cited by 16
“…view is in contrast with our previous interpretation of the mnesic actions of angiotensins on CSM because it contained the concept that memory modulatory systems are endogenous systems that influence memory storage processes (Cahill & McGaugh, 1996; Ferry et al., 1999; Krasne, 1978; McGaugh, 2000).”
Distractible children show abnormal orienting to non-attended auditory stimuli.
Kilpeläinen, R., Luoma, L., Herrgård, E., Sipilä, P., Yppärilä, H., Partanen, J., & Karhu, J. (1999) · NeuroReport · doi:10.1097/00001756-199906230-00013 · Cited by 15
Sex Differences in Locus Coeruleus: A Heuristic Approach That May Explain the Increased Risk of Alzheimer’s Disease in Females
Luckey, A. M., Robertson, I. H., LAWLOR, B. A., Mohan, A., & Vanneste, S. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210404 · Cited by 24
Effects of standardized Ginkgo biloba extract on the acquisition, retrieval and extinction of conditioned suppression: Evidence that short-term memory and long-term memory are differentially modulated
Zamberlam, C. R., Vendrasco, N. C., de Oliveira, D. R., Gaiardo, R. B., & Cerutti, S. M. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.06.036 · Cited by 19
The glucocorticoid response in a free-living bird predicts whether long-lasting memories fade or strengthen with time
Jones, B. C., Bebus, S. E., Ferguson, S. M., Bateman, P. W., & Schoech, S. J. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.10.009 · Cited by 16
Empirical tests of the functional significance of amygdala‐based modulation of hippocampal representations: evidence for multiple memory consolidation pathways
McDonald, R. J., Lo, Q., King, A. L., Wasiak, T. D., & Hong, N. S. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05397.x · Cited by 13
“Multiple pathways for memory modulation The view that memory modulation processes in the mammalian brain are dependent on the amygdala (Cahill & McGaugh, 1996, 1998; Packard & Teather, 1998; McGaugh, 2002, 2005; McGaugh et al., 2002) appears to be a simplified position.”
Background
β1-adrenoceptor expression on GABAergic interneurons in primate dorsolateral prefrontal cortex: potential role in stress-induced cognitive dysfunction
Joyce, M. K. P., Yang, S., Morin, K., Duque, A., Arellano, J. I., Datta, D., Wang, M., & Arnsten, A. F. T. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100628 · Cited by 11
“Exposure to uncontrollable stress impairs the higher cognitive functions of the prefrontal cortex (PFC) in both animals and humans (Murphy et al., 1996; Roozendaal et al., 2004a; Arnsten, 2009; Liston et al., 2009; Qin et al., 2009, 2012; Rinc ´ on-Cort ´ e et al., 2019; Datta and Arnsten, 2019), contributing to risk…”
BackgroundInfluential
Effects of accelerated human music on learning and memory performance of rats
Korsós, G., Horváth, K., Lukács, A., Vezér, T., Glávits, R., Fodor, K., & Fekete, S. (2018) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2018.01.011 · Cited by 15
Non-specific Effect of Fear Conditioning and Specific Effect of Social Defeat on Social Recognition Memory Performance in Female Rats
Penka, L.-L., Bond, T., & Heinrichs, S. (2004) · Stress · doi:10.1080/10253890410001677231 · Cited by 12
“E-mail: stephen.heinrichs@bc.edu stressor exposure are described as “memory modulatory” (McGaugh, 1989; Cahill and McGaugh, 1996; Shors et al., 2000) and are presumably exerted by modifying an underlying arousal state (Deffenbacher, 1983).”
Background
Medial amygdala stimulation produces a long-lasting excitatory postsynaptic potential/spike dissociation in the dentate gyrus in vivo
Noguchi, K., Saitō, H., & Abe, K. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00210-8 · Cited by 10
Interactions between catecholamines and the amygdala in emotional memory: subclinical and clinical evidence.
Cahill, L. (1998) · Advances in Pharmacology · doi:10.1016/s1054-3589(08)60908-4 · Cited by 11
Self-citation
Fear knot
Morrison, P. D., Allardyce, J., & McKane, J. P. (2002) · The British Journal of Psychiatry · doi:10.1192/bjp.180.3.195 · Cited by 10
Drinkers’ memory bias for alcohol picture cues in explicit and implicit memory tasks
Nguyen‐Louie, T. T., Buckman, J. F., Ray, S., & Bates, M. E. (2016) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2015.12.033 · Cited by 9
“Evidence from human and animal studies strongly suggests that emotional memories possess a “privileged status” compared to neutral memories (Cahill and McGaugh, 1995, 1996; Christianson, 1992; LaBar and Cabeza, 2006; Roozendaal, 2000).”
Interaction between midazolam-induced anterograde amnesia and memory enhancement by treatments given immediately after training on an inhibitory avoidance task in rats
Quevedo, J., de-Paris, F., Vianna, M., Barichello, T., Roesler, R., & Kapczinski, F. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200207000-00009 · Cited by 9
Cognitive Behavior Therapy: Implications from Advances in Neuroscience
Bryant, R. A. (2006) · Springer eBooks · doi:10.1007/4-431-29567-4_22 · Cited by 14
Alteration of Human Chorionic Gonadotropin Levels among Pregnant Women with Morning Sickness Attending Antenatal Care Services at Ishaka Adventist Hospital, Uganda
Atusiimirwe, J. K., Eze, E. D., Ezekiel, I., & Rabiu, K. M. (2017) · Journal of Biosciences and Medicines · doi:10.4236/jbm.2017.58005 · Cited by 5
“Furthermore odor information is stored in a long term memory which has strong connections to emotional memory [27].”
Background
Stimulation of Perforant Path Fibers Induces LTP Concurrently in Amygdala and Hippocampus in Awake Freely Behaving Rats
Blaise, J., & Hartman, R. A. (2013) · Journal of Neural Transplantation and Plasticity · doi:10.1155/2013/565167 · Cited by 8
“Emotional memories, including fear conditioning and extinction, are thought to be mediated by the amygdala [10, 18–21].”
Bringing Brain Events to Mind: Functional Systems and Brain Event-Related Potentials
Howard, R. (2001) · Journal of Psychophysiology · doi:10.1027//0269-8803.15.2.69 · Cited by 8
What does the P300 brain response measure in children? New insight from stimulus sequence studies
Kilpeläinen, R., Partanen, J. V., & Karhu, J. (1999) · Neuroreport · doi:10.1097/00001756-199908200-00034 · Cited by 9
Deleterious effect of social instability on broiler chicken learning abilities and behaviour
Arnould, C., Foucher, C., Calandreau, L., Bertin, A., Gigaud, V., & Berri, C. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106398 · Cited by 7
Visitors’ Motives for Attending a Healthy Food Exhibition
Bi, Y., Choi, S., & Kim, I. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17082703 · Cited by 10
“Cahill and McGaugh [68] noted that emotional arousal could affect memory.”
Background
Noise Stress Impairs Prefrontal Cortical Cognitive Function in Monkeys: Evidence for a Hyperdopaminergic Mechanism
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.4.362 · Cited by 6
“These results complement previous studies that show that exposure to acute mild stress has no effect on or actually improves the memory functions associated with the hippocampus and amygdala.(5) Indeed, the absence of stress effects at the very longest delays in the current study (E delays) (Table 1) may be a reflecti…”
Result
When stress enhances memory encoding: The beneficial effects of changing context
Riddell, C. D., Yonelinas, A. P., & Shields, G. S. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107836 · Cited by 6
Memory enhancement produced by post-training exposure to sucrose-conditioned cues
Holahan, M., & White, N. (2013) · F1000Research · doi:10.12688/f1000research.2-22.v1 · Cited by 6
“This analysis revealed a main effect of day (F(2,4) = 56.”
Background
Involvement of the amygdala in the neuroendocrine and behavioral consequences of stress
Akirav, I., & Richter‐Levin, G. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80042-2 · Cited by 6
Bombesin administration impairs memory and does not reverse memory deficit caused by sleep deprivation
Ferreira, L., Oliveira, S. L. B., Raya, J., Esumi, L. A., & Hipólide, D. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.027 · Cited by 5
“The intensity of the shock can be considered a stress factor, since the intensity of the shock is linked to the release of corticosterone, thereby stress is critical to regulating memory formation, with the optimal stress level being beneficial to memory formation [33,34].”

Authors: Cahill, L., & McGaugh, J. L.
Affiliations: University of California, Irvine (US)
Corresponding author: Cahill, Larry
McGaugh, James L
Venue: Current Opinion in Neurobiology
Publisher: Elsevier BV
Published: 1996-04
Volume: 6
Issue: 2
Pages: 237-242
ISSN: 0959-4388 (ISSN-L)
DOI: 10.1016/s0959-4388(96)80078-x
OpenAlex: W2022694793
Cited by: 301
References: 66
Citations by year: 2026: 2 · 2025: 2 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 10 · 2020: 9 · 2019: 5 · 2018: 4 · 2017: 8 · 2016: 13 · 2015: 8 · 2014: 10 · 2013: 9 · 2012: 14
FWCI: 2.29
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Current Opinion in Neurobiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH12526)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: memory modulation, memory storage, emotional memory, stress hormones, sympathoadrenal system, adrenal cortex hormones, hypothalamic-pituitary-adrenal axis, amygdala, emotional arousal
MeSH terms: Adrenal Cortex Hormones, Amygdala, Animals, Brain, Catecholamines, Glucose, Humans, Memory, Peripheral Nerves

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