NEUROBIOLOGY OF THE IMPACT OF AVERSIVE EXPERIENCES ON LEARNING
A SCOPING REVIEW
DOI:
https://doi.org/10.53843/bms.v9i13.576Keywords:
Education, Neurosciences, Learning, Memory, Long-Term, Psychological DistressAbstract
Introduction: The memory processes sustain the activity of learning, which requires attention and directed focus. Classroom aversive experiences such as anxiety disorders, chronic stress and fear can modulate the learning processes. The mechanism consists in a reorientation, mediated by neurohumoral mechanisms, involving the hippocampus and the amygdala, prejudicing the acquisition of knowledge. Method: This study is a scoping review in which the online databases PubMed and LILACS were used to identify papers using an unified search strategy. 18 papers published between 2017 and 2022 composed the scoping review. Result: The selected studies met the eligibility criteria of online availability, traumatic experiences and learning association and correlation between frightening and stressful experiences with memory consolidation. As an acute consequence of stress, high amounts of norepinephrine and cortisol, a glucocorticoid, are released in the body. The interaction between these two agents, especially in the central nervous system, impairs working memory functioning and interrupts the attention functions of the prefrontal cortex, while directing attention only to threatening stimuli, making it hard to non-threatening information consolidation. Chronically, the adverse component is mediated mostly by cortisol, impairing learning through basically two mechanisms. One of them is by disturbing hippocampal functioning and amygdala signaling, leading to long-term memory deficits and facilitating the persistence of fear memories. The other is through avoidance behavior, which works as a defense against unfavorable stimuli, leading the individual to create an obstacle to new learning. Conclusion: In situations of stress, anxiety and fear, there are mechanisms in the hippocampus and amygdala mediated by neurotransmitters and hormones that can impair memory consolidation and prejudice learning.
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References
Ambrose SA, Bridges MW, DiPietro M, Lovett MC, Norman MK. How learning works : seven research-based principles for smart teaching. San Francisco, Ca: Jossey-Bass; 2010.
Vogel S, Schwabe L. Learning and memory under stress: implications for the classroom. npj Science of Learning [Internet]. 2016 Jun 29;1(1). Available from: https://www.nature.com/articles/npjscilearn201611. DOI: https://doi.org/10.1038/npjscilearn.2016.11
Newra Tellechea Rotta, Lygia Ohlweiler, Riesgo S. Transtornos da Aprendizagem. Artmed Editora; 2015.
Takehara-Nishiuchi K. Prefrontal–hippocampal interaction during the encoding of new memories. Brain and Neuroscience Advances. 2020 Jan;4:239821282092558. DOI: https://doi.org/10.1177/2398212820925580
Ozawa T, Ycu EA, Kumar A, Yeh L-F, Ahmed T, Koivumaa J, et al. A feedback neural circuit for calibrating aversive memory strength. Nature Neuroscience. 2016 Nov 14;20(1):90–7. DOI: https://doi.org/10.1038/nn.4439
dos Santos Corrêa M, Vaz B dos S, Menezes BS, Ferreira TL, Tiba PA, Fornari RV. Corticosterone differentially modulates time-dependent fear generalization following mild or moderate fear conditioning training in rats. Neurobiology of Learning and Memory. 2021 Oct;184:107487. DOI: https://doi.org/10.1016/j.nlm.2021.107487
Hagsäter SM, Pettersson R, Holmäng A, Eriksson E. Serotonin depletion reduces both acquisition and expression of context-conditioned fear. Acta Neuropsychiatrica. 2021 Feb 17;33(3):148–55. DOI: https://doi.org/10.1017/neu.2021.3
Moscarello JM, LeDoux J. Diverse Effects of Conditioned Threat Stimuli on Behavior. Cold Spring Harbor Symposia on Quantitative Biology. 2014;79:11–9. DOI: https://doi.org/10.1101/sqb.2014.79.024968
Tyng CM, Amin HU, Saad MNM, Malik AS. The Influences of Emotion on Learning and Memory. Frontiers in Psychology. 2017 Aug 24;8(1454). DOI: https://doi.org/10.3389/fpsyg.2017.01454
Greenspan SI, Beryl Lieff Benderly. The Growth Of The Mind. Da Capo Press, Incorporated; 1997.
Meir Drexler S, Merz CJ, Jentsch VL, Wolf OT. How stress and glucocorticoids timing-dependently affect extinction and relapse. Neuroscience & Biobehavioral Reviews. 2019 Mar;98:145–53. DOI: https://doi.org/10.1016/j.neubiorev.2018.12.029
MCEWEN BS, WEISS JM, SCHWARTZ LS. Selective Retention of Corticosterone by Limbic Structures in Rat Brain. Nature. 1968 Nov;220(5170):911–2. DOI: https://doi.org/10.1038/220911a0
Joëls M, Pu Z, Wiegert O, Oitzl MS, Krugers HJ. Learning under stress: how does it work? Trends in Cognitive Sciences [Internet]. 2006 Apr;10(4):152–8. Available from: https://www.sciencedirect.com/science/article/pii/S1364661306000453 DOI: https://doi.org/10.1016/j.tics.2006.02.002
Pedraza LK, Sierra RO, Crestani AP, Quillfeldt JA, de Oliveira Alvares L. Sequential learning during contextual fear conditioning guides the rate of systems consolidation: Implications for consolidation of multiple memory traces. Hippocampus. 2017 Feb 2;27(5):518–28. DOI: https://doi.org/10.1002/hipo.22708
Brueckner AH, Lass-Hennemann J, Wilhelm FH, Ferreira de Sá DS, Michael T. Cortisol administration after extinction in a fear-conditioning paradigm with traumatic film clips prevents return of fear. Translational Psychiatry. 2019 Apr 8;9(1). DOI: https://doi.org/10.1038/s41398-019-0455-0
Meir Drexler S, Wolf OT. The role of glucocorticoids in emotional memory reconsolidation. Neurobiology of Learning and Memory. 2017 Jul;142:126–34. DOI: https://doi.org/10.1016/j.nlm.2016.11.008
Park HR, Cai M, Yang EJ. Neurogenic Interventions for Fear Memory via Modulation of the Hippocampal Function and Neural Circuits. International Journal of Molecular Sciences. 2022 Mar 25;23(7):3582. DOI: https://doi.org/10.3390/ijms23073582
Wiktorowska L, Bilecki W, Tertil M, Kudla L, Szumiec L, Mackowiak M, et al. Knockdown of the astrocytic glucocorticoid receptor in the central nucleus of the amygdala diminishes conditioned fear expression and anxiety. Behavioural Brain Research [Internet]. 2021 Mar 26 [cited 2021 Mar 31];402:113095. Available from: https://www.sciencedirect.com/science/article/pii/S0166432820307944 DOI: https://doi.org/10.1016/j.bbr.2020.113095
Espejo PJ, Ortiz V, Martijena ID, Molina VA. Stress-induced resistance to fear memory destabilization is associated with an impairment of Lys-48-linked protein polyubiquitination in the Basolateral Amygdala: Influence of D-cycloserine. Neurobiology of Learning and Memory. 2021 Mar;179:107386. DOI: https://doi.org/10.1016/j.nlm.2021.107386
Siddiqui SA, Singh S, Ugale R, Ranjan V, Kanojia R, Saha S, et al. Regulation of HDAC1 and HDAC2 during consolidation and extinction of fear memory. Brain Research Bulletin. 2019 Aug;150:86–101. DOI: https://doi.org/10.1016/j.brainresbull.2019.05.011
Valiati FE, Vasconcelos M, Lichtenfels M, Petry FS, de Almeida RMM, Schwartsmann G, et al. Administration of a Histone Deacetylase Inhibitor into the Basolateral Amygdala Enhances Memory Consolidation, Delays Extinction, and Increases Hippocampal BDNF Levels. Frontiers in Pharmacology [Internet]. 2017 Jun 28 [cited 2019 Nov 23];8. Available from: https://www.frontiersin.org/articles/10.3389/fphar.2017.00415/full DOI: https://doi.org/10.3389/fphar.2017.00415
Nitta Y, Takahashi T, Haitani T, Sugimori E, Kumano H. Avoidance Behavior Prevents Modification of Fear Memory During Reconsolidation. Psychological Reports. 2018 Nov 15;123(2):224–38. DOI: https://doi.org/10.1177/0033294118811116
Gilman TL, Dutta S, Adkins JM, Cecil CA, Jasnow AM. Basolateral amygdala Thy1-expressing neurons facilitate the inhibition of contextual fear during consolidation, reconsolidation, and extinction. Neurobiology of Learning and Memory. 2018 Nov;155:498–507. DOI: https://doi.org/10.1016/j.nlm.2018.09.010
Ito W, Morozov A. Prefrontal-amygdala plasticity enabled by observational fear. Neuropsychopharmacology. 2019 Feb 13;44(10):1778–87. DOI: https://doi.org/10.1038/s41386-019-0342-7
Ponce-Lina R, Serafín N, Carranza M, Arámburo C, Prado-Alcalá RA, Luna M, et al. Differential Phosphorylation of the Glucocorticoid Receptor in Hippocampal Subregions Induced by Contextual Fear Conditioning Training. Frontiers in Behavioral Neuroscience. 2020 Feb 13;14. DOI: https://doi.org/10.3389/fnbeh.2020.00012
Schafe GE, LeDoux JE. Memory Consolidation of Auditory Pavlovian Fear Conditioning Requires Protein Synthesis and Protein Kinase A in the Amygdala. The Journal of Neuroscience. 2000 Sep 15;20(18):RC96–6. DOI: https://doi.org/10.1523/JNEUROSCI.20-18-j0003.2000
Barsegyan A, Mackenzie SM, Kurose BD, McGaugh JL, Roozendaal B. Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proceedings of the National Academy of Sciences [Internet]. 2010 Sep 1;107(38):16655–60. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2944727/ DOI: https://doi.org/10.1073/pnas.1011975107
de Medeiros Gabriela F, Lafenêtre P, Janthakhin Y, Cerpa J-C, Zhang C-L, Mehta Marishka M, et al. Corticosteroid-Binding Globulin Deficiency Specifically Impairs Contextual and Recognition Memory Consolidation in Male Mice. Neuroendocrinology. 2019;109(4):322–32. DOI: https://doi.org/10.1159/000499827
Woo H, Hong CJ, Jung S, Choe S, Yu S-W. Chronic restraint stress induces hippocampal memory deficits by impairing insulin signaling. Molecular Brain. 2018 Jul 3;11(1). DOI: https://doi.org/10.1186/s13041-018-0381-8
Zhao W-Q, Alkon DL. Role of insulin and insulin receptor in learning and memory. Molecular and Cellular Endocrinology [Internet]. 2001 May 25;177(1):125–34. Available from: https://www.sciencedirect.com/science/article/pii/S0303720701004555 DOI: https://doi.org/10.1016/S0303-7207(01)00455-5
Belleau EL, Treadway MT, Pizzagalli DA. The Impact of Stress and Major Depressive Disorder on Hippocampal and Medial Prefrontal Cortex Morphology. Biological Psychiatry. 2019 Mar;85(6):443–53. DOI: https://doi.org/10.1016/j.biopsych.2018.09.031
Wang Z, Neylan TC, Mueller SG, Lenoci M, Truran D, Marmar CR, et al. Magnetic Resonance Imaging of Hippocampal Subfields in Posttraumatic Stress Disorder. Archives of General Psychiatry [Internet]. 2010 Mar 1 [cited 2021 Apr 18];67(3):296–303. Available from: https://jamanetwork.com/journals/jamapsychiatry/article-abstract/210641 DOI: https://doi.org/10.1001/archgenpsychiatry.2009.205
Merino JJ, Muñetón-Gomez V, Muñetón-Gómez C, Pérez-Izquierdo MÁ, Loscertales M, Toledano Gasca A. Hippocampal CCR5/RANTES Elevations in a Rodent Model of Post-Traumatic Stress Disorder: Maraviroc (a CCR5 Antagonist) Increases Corticosterone Levels and Enhances Fear Memory Consolidation. Biomolecules. 2020 Feb 1;10(2):212. DOI: https://doi.org/10.3390/biom10020212
Yu J, Naoi T, Sakaguchi M. Fear generalization immediately after contextual fear memory consolidation in mice. Biochemical and Biophysical Research Communications. 2021 Jun;558:102–6. DOI: https://doi.org/10.1016/j.bbrc.2021.04.072
Schmidt SD, Furini CRG, Zinn CG, Cavalcante LE, Ferreira FF, Behling JAK, et al. Modulation of the consolidation and reconsolidation of fear memory by three different serotonin receptors in hippocampus. Neurobiology of Learning and Memory. 2017 Jul;142:48–54. DOI: https://doi.org/10.1016/j.nlm.2016.12.017
Kamada S, Nagayama T. Anxiety induces long-term memory forgetting in the crayfish. Journal of Comparative Physiology A. 2021 Apr 21;207(4):459–67. DOI: https://doi.org/10.1007/s00359-021-01487-1
Roozendaal B, Hermans EJ. Norepinephrine effects on the encoding and consolidation of emotional memory: improving synergy between animal and human studies. Current Opinion in Behavioral Sciences. 2017 Apr;14:115–22. DOI: https://doi.org/10.1016/j.cobeha.2017.02.001
Williamson JB, Porges EC, Lamb DG, Porges SW. Maladaptive autonomic regulation in PTSD accelerates physiological aging. Frontiers in Psychology. 2015 Jan 21;5. DOI: https://doi.org/10.3389/fpsyg.2014.01571
Vedhara K, Hyde J, Gilchrist ID, Tytherleigh M, Plummer S. Acute stress, memory, attention and cortisol. Psychoneuroendocrinology. 2000 Aug;25(6):535–49. DOI: https://doi.org/10.1016/S0306-4530(00)00008-1
Oei NYL, Everaerd WTAM, Elzinga BM, van Well S, Bermond B. Psychosocial stress impairs working memory at high loads: An association with cortisol levels and memory retrieval. Stress. 2006 Jan;9(3):133–41. DOI: https://doi.org/10.1080/10253890600965773
Rued HA, Hilmert CJ, Strahm AM, Thomas LE. The influence of stress on attentional bias to threat: An angry face and a noisy crowd. Psychonomic Bulletin & Review. 2018 Oct 23;26(3):943–50. DOI: https://doi.org/10.3758/s13423-018-1538-2
Schwabe L, Wolf OT. Learning under stress impairs memory formation. Neurobiology of Learning and Memory. 2010 Feb;93(2):183–8. DOI: https://doi.org/10.1016/j.nlm.2009.09.009
SHIN LM. Amygdala, Medial Prefrontal Cortex, and Hippocampal Function in PTSD. Annals of the New York Academy of Sciences. 2006 Jul 1;1071(1):67–79. DOI: https://doi.org/10.1196/annals.1364.007
Joëls M, Karst H, Alfarez D, Heine VM, Qin Y, Riel E van, et al. Effects of Chronic Stress on Structure and Cell Function in Rat Hippocampus and Hypothalamus. Stress. 2004 Dec;7(4):221–31. DOI: https://doi.org/10.1080/10253890500070005
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