Adult-Onset Hypothyroidism Enhances Fear Memory and Upregulates Mineralocorticoid and Glucocorticoid Receptors in the Amygdala
Open accessAbstract
Hypothyroidism is the most common hormonal disease in adults, which is frequently accompanied by learning and memory impairments and emotional disorders. However, the deleterious effects of thyroid hormones deficiency on emotional memory are poorly understood and often underestimated. To evaluate the consequences of hypothyroidism on emotional learning and memory, we have performed a classical Pavlovian fear conditioning paradigm in euthyroid and adult-thyroidectomized Wistar rats. In this experimental model, learning acquisition was not impaired, fear memory was enhanced, memory extinction was delayed and spontaneous recovery of fear memory was exacerbated in hypothyroid rats. The potentiation of emotional memory under hypothyroidism was associated with an increase of corticosterone release after fear conditioning and with higher expression of glucocorticoid and mineralocorticoid receptors in the lateral and basolateral nuclei of the amygdala, nuclei that are critically involved in the circuitry of fear memory. Our results demonstrate for the first time that adult-onset hypothyroidism potentiates fear memory and also increases vulnerability to develop emotional memories. Furthermore, our findings suggest that enhanced corticosterone signaling in the amygdala is involved in the pathophysiological mechanisms of fear memory potentiation. Therefore, we recommend evaluating whether inappropriate regulation of fear in patients with post-traumatic stress and other mental disorders is associated with abnormal levels of thyroid hormones, especially those patients refractory to treatment.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Previous studies have described a role for thyroid hormone signaling in the amygdala in regulating fear learning and in the MeA specifically in modulating social vigilance.
“Previous studies have described a role for thyroid hormone signaling in the amygdala in regulating fear learning [78,79] and in the MeA specifically in modulating social vigilance [80].”
From Rapid changes in plasma corticosterone and medial amygdala transcriptome profiles during social status change reveal molecular pathways associated with a major life history transition in mouse dominance hierarchies (2025) · cites this paper as [79]
The Introduction and Discussion (pages unavailable) link thyroid hormone status and amygdala changes to fear conditioning, and report enhanced fear memory and delayed extinction in hypothyroid rats. The Discussion also says initial learning of the aversive association was unaffected, so the paper supports a role in fear-memory processing rather than a general effect on fear learning. The separate MeA/social-vigilance clause is cited to [80], not this source. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Context and Behavioral Processes in Extinction: Table 1.
Bouton, M. E. (2004) · Learning & Memory · doi:10.1101/lm.78804 · Cited by 1,808 · see citing works
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543 · see citing works
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Adrenal steroid receptors and actions in the nervous system
McEwen, B. S., de Kloet, E. R., & Rostène, W. H. (1986) · Physiological Reviews · doi:10.1152/physrev.1986.66.4.1121 · Cited by 1,238 · see citing works
Werner & Ingbar's the thyroid : a fundamental and clinical text
Werner, S. C., Ingbar, S. H., Braverman, L. E., & Utiger, R. D. (2012) · Lippincott-Raven eBooks · Cited by 1,016 · see citing works
Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala
Fanselow, M. S., & LeDoux, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)80775-8 · Cited by 914 · see citing works
The role of thyroid hormones in prenatal and neonatal neurological development--current perspectives
Porterfield, S. P. (1993) · Endocrine Reviews · doi:10.1210/er.14.1.94 · Cited by 679 · see citing works
De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder.
Orr, S. P., Metzger, L. J., Lasko, N. B., Macklin, M. L., Peri, T., & Pitman, R. K. (2000) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.109.2.290 · Cited by 653 · see citing works
Roberts, C. G., & Ladenson, P. W. (2004) · The Lancet · doi:10.1016/s0140-6736(04)15696-1 · Cited by 567 · see citing works
The conditioned emotional response as a function of intensity of the US.
Annau, Z., & Kamin, L. J. (1961) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0042199 · Cited by 563 · see citing works
The Influence of Stress Hormones on Fear Circuitry
Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135620 · Cited by 556 · see citing works
Bradley, D. J., Towle, H. C., & Young, W. S. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-06-02288.1992 · Cited by 530 · see citing works
Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.017 · Cited by 512 · see citing works
Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies
Hamilton, J. P., Siemer, M., & Gotlib, I. H. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.57 · Cited by 492 · see citing works
Applying Learning Principles to the Treatment of Post‐Trauma Reactions
ROTHBAUM, B. O., & DAVIS, M. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1301.012 · Cited by 454 · see citing works
Naloxone and shock-elicited freezing in the rat.
Fanselow, M. S., & Bolles, R. C. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077609 · Cited by 411 · see citing works
de Escobar, G. M., PASTOR, R., Obregón, M.-J., & del Rey, F. E. (1985) · Endocrinology · doi:10.1210/endo-117-5-1890 · Cited by 361 · see citing works
Epidemiology and prevention of clinical and subclinical hypothyroidism.
Vanderpump, M. P. J., & Tunbridge, W. M. G. (2002) · Thyroid · doi:10.1089/105072502761016458 · Cited by 347 · see citing works
Roozendaal, B., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0001 · Cited by 317 · see citing works
Werner and Ingbar's The Thyroid: A Fundamental and Clinical Text
(1992) · Annals of Internal Medicine · doi:10.7326/0003-4819-117-6-541_8 · Cited by 302 · see citing works
Criteria for rationally evaluating animal models of postraumatic stress disorder
Yehuda, R., & Antelman, S. M. (1993) · Biological Psychiatry · doi:10.1016/0006-3223(93)90001-t · Cited by 301 · see citing works
Perspectives in the Study of Thyroid Hormone Action on Brain Development and Function
Bernal, J., Guadaño‐Ferraz, A., & Morte, B. (2003) · Thyroid · doi:10.1089/105072503770867174 · Cited by 287 · see citing works
Self-citationThe Role of Thyroid Hormones in Prenatal and Neonatal Neurological Development—Current Perspectives
Porterfield, S. P., & Hendrich, C. E. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-1-94 · Cited by 283 · see citing works
Neurocognitive Aspects of Hypothyroidism
Dugbartey, A. T. (1998) · Archives of Internal Medicine · doi:10.1001/archinte.158.13.1413 · Cited by 252 · see citing works
Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain
Desouza, L. A., Ladiwala, U., Daniel, S. M., Agashe, S., Vaidya, R. A., & Vaidya, V. A. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.03.010 · Cited by 231 · see citing works
Morte, B., Manzano, J., Scanlan, T. S., Vennström, B., & Bernal, J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062413299 · Cited by 227 · see citing works
Venero, C., Guadaño‐Ferraz, A., Herrero, A. I., Nordström, K., Manzano, J., de Escobar, G. M., Bernal, J., & Vennström, B. (2005) · Genes & Development · doi:10.1101/gad.346105 · Cited by 222 · see citing works
Self-citationYang, Y.-L., Chao, P.-K., & Lu, K. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300899 · Cited by 216 · see citing works
Hypothyroidism and depression. Evidence from complete thyroid function evaluation
Gold, M. S. (1981) · JAMA · doi:10.1001/jama.245.19.1919 · Cited by 204 · see citing works
Cordero, M. I., Merino, J. J., & Sandi, C. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.4.885 · Cited by 203 · see citing works
Toward an Animal Model of Posttraumatic Stress Disorder
Siegmund, A., & Wotjak, C. T. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1364.025 · Cited by 199 · see citing works
Cordero, M. I., Venero, C., Kruyt, N. D., & Sandi, C. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00160-0 · Cited by 182 · see citing works
Self-citationDevelopment of a Panel of Monoclonal Antibodies against the Mineralocorticoid Receptor
Gómez-Sánchez, C. E., de Rodriguez, A. F., Romero, D. G., Estess, J., Warden, M. P., Gomez-Sanchez, M. T., & Gómez-Sánchez, E. P. (2005) · Endocrinology · doi:10.1210/en.2005-0860 · Cited by 182 · see citing works
Guadaño‐Ferraz, A., Escamez, M. J., Rausell, E., & Bernal, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03430.1999 · Cited by 180 · see citing works
Self-citationCordero, M. I., Merino, J. J., & Sandi, C. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.4.885 · Cited by 173 · see citing works
Montero‐Pedrazuela, A., Venero, C., Lavado-Autric, R., Fernández‐Lamo, I., García‐Verdugo, J. M., Bernal, J., & Guadaño‐Ferraz, A. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001802 · Cited by 171 · see citing works
Self-citationHui, G. K. (2003) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2003.09.002 · Cited by 168 · see citing works
Gerges, N. Z., Stringer, J. L., & Alkadhi, K. A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03181-x · Cited by 155 · see citing works
Alzoubi, K. H., Gerges, N. Z., Aleisa, A. M., & Alkadhi, K. A. (2008) · Hippocampus · doi:10.1002/hipo.20476 · Cited by 144 · see citing works
Yang, R. J., Mozhui, K., Karlsson, R.-M., Cameron, H. A., Williams, R. W., & Holmes, A. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301665 · Cited by 143 · see citing works
Cell-specific effects of thyroid hormone on RC3/neurogranin expression in rat brain
Iñiguez, M. A., de Lecea, L., Guadaño‐Ferraz, A., Morte, B., Gerendasy, D. D., Sutcliffe, J. G., & Bernal, J. (1996) · Endocrinology · doi:10.1210/endo.137.3.8603571 · Cited by 137 · see citing works
Self-citationThyroid Hormones Affect Neurogenesis in the Dentate Gyrus of Adult Rat
Ambrogini, P., Cuppini, R., Ferri, P., Mancini, C., Ciaroni, S., Voci, A., Gerdoni, E., & Gallo, G. (2005) · Neuroendocrinology · doi:10.1159/000087648 · Cited by 136 · see citing works
Hypothyroidism and Cognition: Preliminary Evidence for a Specific Defect in Memory
Burmeister, L. A., Ganguli, M., Dodge, H. H., Toczek, T., DeKosky, S. T., & Nebes, R. D. (2001) · Thyroid · doi:10.1089/10507250152741037 · Cited by 132 · see citing works
Guadaño‐Ferraz, A., Benavides‐Piccione, R., Venero, C., Lancha, C., Vennström, B., Sandi, C., DeFelipe, J., & Bernal, J. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001196 · Cited by 111 · see citing works
Self-citationThyroid hormone regulation by stress and behavioral differences in adult male rats
Helmreich, D. L., & Tylee, D. S. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.06.003 · Cited by 103 · see citing works
Duntas, L. H., & Biondi, B. (2007) · European Journal of Endocrinology · doi:10.1530/eje.1.02310 · Cited by 98 · see citing works
IRANMANESH, A., LIZARRALDE, G., JOHNSON, M. L., & VELDHUIS, J. D. (1990) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-70-1-155 · Cited by 93 · see citing works
López‐Fernández, M. A., Montaron, M., Varea, E., Rougon, G. N., Venero, C., Abrous, D. N., & Sandi, C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0396-07.2007 · Cited by 86 · see citing works
Self-citationDíez, D., Grijota-Martínez, C., Agretti, P., Marco, G. D., Tonacchera, M., Pinchera, A., de Escobar, G. M., Bernal, J., & Morte, B. (2008) · Endocrinology · doi:10.1210/en.2008-0350 · Cited by 79 · see citing works
Zorawski, M. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4075 · Cited by 72 · see citing works
Immunocytochemical Localization of Thyroid Hormone Receptors in the Adult Rat Brain
Puymirat, J., Miehe, M., Marchand, R., Sarliève, L. L., & Dussault, J. H. (1991) · Thyroid · doi:10.1089/thy.1991.1.173 · Cited by 70 · see citing works
Response inhibition in Extinction
Rescorla, R. A. (2010) · doi:10.1080/713932655 · Cited by 70 · see citing works
Wang, S., & Mason, J. W. (1999) · Psychosomatic Medicine · doi:10.1097/00006842-199903000-00001 · Cited by 68 · see citing works
García‐Segura, L. M. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195326611.001.0001 · Cited by 67 · see citing works
Bauer, M., Priebe, S., Kürten, I., Gräf, K.-J., & Baumgartner, A. (1994) · Psychiatry Research · doi:10.1016/0165-1781(94)90047-7 · Cited by 66 · see citing works
Fernández‐Lamo, I., Montero‐Pedrazuela, A., Delgado-Garcia, J. M., Guadaño‐Ferraz, A., & Gruart, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06862.x · Cited by 64 · see citing works
Self-citationPresence of L-Thyroxine and 3,5,3′-Triiodo-L-thyronine in Tissues from Thyroidectomized Rats*
Obregón, M.-J., Mallol, J., del Rey, F. E., & de Escobar, G. M. (1981) · Endocrinology · doi:10.1210/endo-109-3-908 · Cited by 64 · see citing works
Ruiz‐Marcos, A., Abella, P. C., Garc�a, A. G., del Rey, F. E., & de Escobar, G. M. (1988) · Experimental Brain Research · doi:10.1007/bf00406617 · Cited by 60 · see citing works
Sadow, P. M., Chassande, O., Koo, E. K., Gauthier, K. C., Samarut, J., Xu, J., O’Malley, B. W., & Weiss, R. E. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(03)00122-9 · Cited by 58 · see citing works
Rat Brain Type II 5′‐Iodothyronine Deiodinase Activity Is Extremely Sensitive to Stress
Baumgartner, A., Hiedra, L., Pinna, G., Eravci, M., Prengel, H., & MEINHOLD, H. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.71020817.x · Cited by 53 · see citing works
Verbal Memory Retrieval Deficits Associated With Untreated Hypothyroidism
Miller, K. J., Parsons, T. D., Whybrow, P. C., Van Herle, K., Rasgon, N., Van Herle, A., Martinez, D., Silverman, D. H., & Bauer, M. (2007) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.2007.19.2.132 · Cited by 52 · see citing works
The Thyroid. A Fundamental and Clinical Text
Hollenhorst, R. W. (1972) · American Journal of Ophthalmology · doi:10.1016/0002-9394(72)90152-3 · Cited by 51 · see citing works
Sui, L., Wang, F., & Li, B. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.042 · Cited by 46 · see citing works
Metyrapone Reveals That Previous Chronic Stress Differentially Impairs Hippocampal-dependent Memory
Conrad, C. D., Mauldin-Jourdain, M. L., & Hobbs, R. J. (2001) · Stress · doi:10.3109/10253890109014754 · Cited by 41 · see citing works
Constantinou, C., Margarity, M., & Valcana, T. (2005) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-005-6934-z · Cited by 41 · see citing works
Sarabdjitsingh, R. A., Meijer, O. C., & de Kloet, E. R. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.052 · Cited by 40 · see citing works
Thyroid Hormone Action on ACTH Secretion
Sánchez‐Franco, F., Fernández‐Pérez, L., Fernández, G., & Cacicedo, L. (1989) · Hormone and Metabolic Research · doi:10.1055/s-2007-1009285 · Cited by 40 · see citing works
Analysis of Thyroid Hormone-Dependent Genes in the Brain by In Situ Hybridization
Bernal, J., & Guadaño‐Ferraz, A. (2003) · Humana Press eBooks · doi:10.1385/1-59259-174-4:71 · Cited by 26 · see citing works
Self-citationThyroid Hormones and Brain Development
Bernal, J. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50076-7 · Cited by 24 · see citing works
Thyroid hormone levels and psychological symptoms in sexually abused adolescent girls
Haviland, M. G., Sonne, J. L., Anderson, D. L., Nelson, J. C., Sheridan-Matney, C., Nichols, J. G., Carlton, E. I., & Murdoch, W. G. C. (2006) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2005.11.011 · Cited by 21 · see citing works
Pharmacological Effects of Propylthiouracil on Corticosterone Secretion in Male Rats
Lo, M. J., Wang, S. W., Kau, M., Chen, J. J., Chen, Y. H., Fang, V. S., Ho, L. T., & Wang, P. S. (1998) · Journal of Investigative Medicine · doi:10.1177/108155899804600906 · Cited by 19 · see citing works
Behavior therapy and the philosophers
Eysenck, H. J. (1979) · Behaviour Research and Therapy · doi:10.1016/0005-7967(79)90067-6 · Cited by 19 · see citing works
Effect of the 2004 Mid Niigata Prefecture Earthquake on Patients with Endocrine Disorders
Kamoi, K., Tanaka, M., Ikarashi, T., & 宮腰, 将. (2006) · Endocrine Journal · doi:10.1507/endocrj.k06-022 · Cited by 10 · see citing works
Lee, E., Kim, H., Im, J. Y., Kim, J., Park, H.-Y., Ryu, J. Y., Lee, J., Shim, K. A., Jung, K. K., Han, S. Y., et al. (2008) · The Journal of Toxicological Sciences · doi:10.2131/jts.33.299 · Cited by 10 · see citing works
Flagged first, then by citations
2 of the 82 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [43]Bouton ME 2004 Context and behavioral processes in extinction. Learn Mem 11 485 494 15466298
Cited by
Sorted by citations
Porcu, E., Medici, M., Pistis, G., Volpato, C. B., Wilson, S. G., Cappola, A. R., Bos, S. D., Deelen, J., den Heijer, M., Freathy, R. M., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003266 · Cited by 229 · see citing works
Treatment-refractory posttraumatic stress disorder (TRPTSD): a review and framework for the future
Koek, R. J., Schwartz, H. N., Scully, S., Langevin, J., Spangler, S. L., Korotinsky, A., Jou, K., & Leuchter, A. F. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.01.015 · Cited by 70 · see citing works
Thyroid hormones regulate anxiety in the male mouse
Buras, A. B., Battle, L., Landers, E., Nguyen, T. T., & Vasudevan, N. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.11.008 · Cited by 53 · see citing works
Increased anxiety and fear memory in adult mice lacking type 2 deiodinase
Bárez-López, S., Montero-Pedrazuela, A., Bosch-García, D., Venero, C., & Guadaño-Ferraz, A. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.013 · Cited by 50 · see citing works
Self-citationGe, J., Peng, Y., Qi, C., Chen, F.-H., & Zhou, J. (2013) · Endocrine · doi:10.1007/s12020-013-0001-4 · Cited by 47 · see citing works
Malikowska‐Racia, N., & Sałat, K. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.02.001 · Cited by 46 · see citing works
MicroRNA regulation of persistent stress-enhanced memory
Daws, S. E., Jamieson, S., de Nijs, L., Jones, M., Snijders, C., Klengel, T., Joseph, N. F., Krauskopf, J., Kleinjans, J. C. S., Vinkers, C. H., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0432-2 · Cited by 44 · see citing works
Endocrine factors in key structural and intracellular changes in depression
Gold, P. W. (2021) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2021.01.003 · Cited by 35 · see citing works
Thyroid hormones and learning-associated neuroplasticity
Raymaekers, S. R., & Darras, V. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.04.001 · Cited by 33 · see citing works
Sabatino, L., Lapi, D., & Seppia, C. D. (2024) · Biomolecules · doi:10.3390/biom14020198 · Cited by 30 · see citing works
Dynamic Patterns of Threat-Associated Gene Expression in the Amygdala and Blood
Lori, A., Maddox, S. A., Sharma, S. K., Andero, R., Ressler, K. J., & Smith, A. K. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00778 · Cited by 26 · see citing works
Reverte, I., Pujol, A., Domingo, J. L., & Colomina, M. T. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.05.013 · Cited by 18 · see citing works
Hipolito, L. T. M., Batista, T. H., dos Anjos‐Garcia, T., Giusti‐Paiva, A., & Vilela, F. C. (2022) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10243 · Cited by 9 · see citing works
Brčić, L., Gračan, S., Barić, A., Gunjača, I., Lovrić, V. T., Kolčić, I., Zemunik, T., Polašek, O., Barbalić, M., Punda, A., et al. (2017) · Immunological Investigations · doi:10.1080/08820139.2017.1337785 · Cited by 8 · see citing works
Milewski, T. M., Lee, W., Young, R. L., Hofmann, H. A., & Curley, J. P. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011548 · Cited by 7 · see citing works
Hippocampal Administration of Levothyroxine Impairs Contextual Fear Memory Consolidation in Rats
Yu, D., Zhou, H., Zou, L., Jiang, Y. L., Wu, X., Jiang, L., Zhou, Q., Yang, Y., Xu, L., & Mao, R. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00223 · Cited by 7 · see citing works
Ibrahim, N., Diab, M., Hassan, A., Anwar, H. M., Ragab, W. M., Morsi, E., Diab, M., Boushra, A. F., & Sadek, N. A. (2023) · AL-Kindy College Medical Journal · doi:10.47723/kcmj.v19i1.920 · Cited by 7 · see citing works
Memory impairments in rodent depression models: A link with depression theories
Sałaciak, K., Koszałka, A., Lustyk, K., Żmudzka, E., Jagielska, A., & Pytka, K. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110774 · Cited by 6 · see citing works
Synaptic Plasticity and Cognitive Ability in Experimental Adult-Onset Hypothyroidism
Alkadhi, K. A. (2024) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.123.001887 · Cited by 6 · see citing works
Can Hypothyroidism Cause Acute Central Serous Chorioretinopathy?
Ulaş, F., Uyar, E., Tekçe, H., & Çelebi, S. (2019) · Seminars in Ophthalmology · doi:10.1080/08820538.2019.1684524 · Cited by 5 · see citing works
Mohamed, D., & Ahmed, S. M. (2018) · The Egyptian Journal of Histology · doi:10.21608/ejh.2018.3807.1008 · Cited by 4 · see citing works
Voicu, S. N., Scărlătescu, A. I., Apetroaei, M.-M., Nedea, M. I., Blejan, I. E., Udeanu, D. I., Velescu, B. Ș., Ghica, M., Nedea, O. A., Cobelschi, C., et al. (2024) · Nutrients · doi:10.3390/nu16071077 · Cited by 6 · see citing works
Potential of Heterogeneous Compounds as Antidepressants: A Narrative Review
Hu, G., Zhang, M., Wang, Y., Yu, M., & Zhou, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232213776 · Cited by 4 · see citing works
Functional (Psychogenic) Seizures are Associated with Thyroid Disorders
Asadi‐Pooya, A. A., & Farazdaghi, M. (2022) · Heart and Mind · doi:10.4103/hm.hm_37_21 · Cited by 2 · see citing works
Milewski, T., Lee, W., Rada, K. R., & Curley, J. P. (2025) · bioRxiv · doi:10.1111/ejn.70295 · Cited by 1 · see citing works
Hallab, A., & Initiative, A. D. N. (2024) · medRxiv · doi:10.1101/2024.10.02.24314757
Huang, Z., Zheng, Y., Hu, Y., Wang, X., Qi, X., & Guo, S. (2025) · Neurological Research · doi:10.1080/01616412.2025.2591840
Organizational impacts of hypothyroidism on behavior
Northcutt, K. V. (2026) · Hormones and Behavior · doi:10.1016/j.yhbeh.2026.105983
- Authors
- Montero-Pedrazuela, A., Fernández-Lamo, I., Alieva, M., Pereda-Pérez, I., Venero, C., & Guadaño-Ferraz, A.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Universidad Nacional de Educación a Distancia (ES)
- Corresponding author
- Venero, César
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-10-24
- Volume
- 6
- Issue
- 10
- Pages
- e26582
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3200331
- OpenAlex
- W2058936529
- Cited by
- 30
- References
- 82
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 1 · 2019: 5 · 2018: 1 · 2017: 4 · 2016: 1 · 2014: 2 · 2013: 3
- FWCI
- 0.81
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ministerio de Ciencia e Innovación (SAF2009-09129)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- adult-onset hypothyroidism, fear memory, amygdala, mineralocorticoid receptor, glucocorticoid receptor, corticosterone, thyroidectomy, fear extinction, memory extinction, emotional memory, post-traumatic stress disorder, thyroid hormones
- MeSH terms
- Adult, Amygdala, Animals, Fear, Humans, Hypothyroidism, Memory, Receptors, Glucocorticoid, Age of Onset, Receptors, Mineralocorticoid, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review