Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress
Open accessAbstract
We report that 9 d of uncontrolled experimental diabetes induced by streptozotocin (STZ) in rats is an endogenous chronic stressor that produces retraction and simplification of apical dendrites of hippocampal CA3 pyramidal neurons, an effect also observed in nondiabetic rats after 21 d of repeated restraint stress or chronic corticosterone (Cort) treatment. Diabetes also induces morphological changes in the presynaptic mossy fiber terminals (MFT) that form excitatory synaptic contacts with the proximal CA3 apical dendrites. One effect, synaptic vesicle depletion, occurs in diabetes as well as after repeated stress and Cort treatment. However, diabetes produced other MFT structural changes that differ qualitatively and quantitatively from other treatments. Furthermore, whereas 7 d of repeated stress was insufficient to produce dendritic or synaptic remodeling in nondiabetic rats, it potentiated both dendritic atrophy and MFT synaptic vesicle depletion in STZ rats. These changes occurred in concert with adrenal hypertrophy and elevated basal Cort release as well as hypersensitivity and defective shutoff of Cort secretion after stress. Thus, as an endogenous stressor, STZ diabetes not only accelerates the effects of exogenous stress to alter hippocampal morphology; it also produces structural changes that overlap only partially with those produced by stress and Cort in the nondiabetic state.
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?
Animals with abnormal glucose metabolism have more hippocampal damage when exposed to high levels of corticosteroids.
“which may help explain why animals that have abnormal glucose metabolism have more hippocampal damage when exposed to high levels of corticosteroids (20).”
From Reduced glucose tolerance is associated with poor memory performance and hippocampal atrophy among normal elderly (2003) · cites this paper as [20]
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
Protective and Damaging Effects of Stress Mediators
McEwen, B. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801153380307 · Cited by 6,733 · see citing works
Self-citationMcEwen, B. S. (1993) · Archives of Internal Medicine · doi:10.1001/archinte.153.18.2093 · Cited by 4,365 · see citing works
Self-citationPhysiological functions of glucocorticoids in stress and their relation to pharmacological actions
MUNCK, A., GUYRE, P. M., & HOLBROOK, N. J. (1984) · Endocrine Reviews · doi:10.1210/edrv-5-1-25 · Cited by 3,083 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
Self-citationHippocampal atrophy in recurrent major depression
Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.3908 · Cited by 1,932 · see citing works
Cortisol levels during human aging predict hippocampal atrophy and memory deficits
Lupien, S. J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N. P. V., Thakur, M., McEwen, B. S., Hauger, R. L., & Meaney, M. J. (1998) · Nature Neuroscience · doi:10.1038/271 · Cited by 1,653 · see citing works
Self-citation(1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.7.973 · Cited by 1,610 · see citing works
Handbook of Life Stress, Cognition and Health
PASTOR, L. H. (1989) · American Journal of Psychiatry · doi:10.1176/ajp.146.10.1347 · Cited by 1,402 · see citing works
Synaptic Vesicle Phosphoproteins and Regulation of Synaptic Function
Greengard, P., Valtorta, F., Czernik, A. J., & Benfenati, F. (1993) · Science · doi:10.1126/science.8430330 · Cited by 1,311 · see citing works
Corticosteroid inhibition of acth secretion
KELLER-WOOD, M. E., & DALLMAN, M. F. (1984) · Endocrine Reviews · doi:10.1210/edrv-5-1-1 · Cited by 1,219 · see citing works
Diabetogenic action of streptozotocin: relationship of dose to metabolic response
Junod, A. F., Lambert, A. E., Stauffacher, W., & Renold, A. E. (1969) · Journal of Clinical Investigation · doi:10.1172/jci106180 · Cited by 931 · see citing works
Gurvits, T. V., Shenton, M. E., Hokama, H., Ohta, H., Lasko, N. B., Gilbertson, M. W., Orr, S. P., Kikinis, R., Jolesz, F. A., McCarley, R. W., et al. (1996) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00229-6 · Cited by 899 · see citing works
Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity.
Sibson, N. R., Dhankhar, A., Mason, G. F., Rothman, D. L., Behar, K. L., & Shulman, R. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.316 · Cited by 897 · see citing works
Rosmond, R., Dallman, M. F., & Björntorp, P. A. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.6.4843 · Cited by 892 · see citing works
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Self-citationMagarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00259-l · Cited by 863 · see citing works
Self-citationStarkman, M. N., Gebarski, S. S., Berent, S., & Schteingart, D. E. (1992) · Biological Psychiatry · doi:10.1016/0006-3223(92)90079-f · Cited by 840 · see citing works
(1992) · Cited by 777 · see citing works
DRUGS PRODUCING DIABETES THROUGH DAMAGE OF THE INSULIN SECRETING CELLS
Rerup, C. (1970) · Pharmacological Reviews · doi:10.1016/s0031-6997(25)06885-1 · Cited by 731 · see citing works
Moderate hyperglycemia augments ischemic brain damage
Pulsinelli, W. A., Waldman, S., Rawlinson, D. G., & Plum, F. (1982) · Neurology · doi:10.1212/wnl.32.11.1239 · Cited by 725 · see citing works
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.902 · Cited by 664 · see citing works
Self-citationConrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.902 · Cited by 663 · see citing works
Self-citationChronic stress alters synaptic terminal structure in hippocampus
Magariños, A. M., Verdugo, J. M. G., & McEwen, B. S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14002 · Cited by 543 · see citing works
Self-citationDistinct pools of synaptic vesicles in neurotransmitter release
Pieribone, V. A., Shupliakov, O., Brodin, L., Hilfiker, S., Czernik, A. J., & Greengard, P. (1995) · Nature · doi:10.1038/375493a0 · Cited by 532 · see citing works
Biessels, G. J., Kamal, A., Urban, I. J. A., Spruijt, B. M., Erkelens, D. W., & Gispen, W. H. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00510-1 · Cited by 379 · see citing works
Cerebral function in diabetes mellitus
Biessels, G. J., Kappelle, A. C., Bravenboer, B., Erkelens, D. W., & Gispen, W. H. (1994) · Diabetologia · doi:10.1007/bf00417687 · Cited by 341 · see citing works
The Impact of Diabetes on the CNS
McCall, A. L. (1992) · Diabetes · doi:10.2337/diab.41.5.557 · Cited by 341 · see citing works
Magariños, A. M., Deslandes, A., & McEwen, B. S. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00163-6 · Cited by 330 · see citing works
Self-citationEnhancement of some 5-HT-dependent behavioural responses following repeated immobilization in rats
Kennett, G. A., Dickinson, S. L., & Curzon, G. (1985) · Brain Research · doi:10.1016/0006-8993(85)90684-5 · Cited by 254 · see citing works
Blood-Brain Glucose Transfer: Repression in Chronic Hyperglycemia
Gjedde, A., & Crone, C. (1981) · Science · doi:10.1126/science.7027439 · Cited by 235 · see citing works
Mordes, J. P., & Rossini, A. A. (1981) · The American Journal of Medicine · doi:10.1016/0002-9343(81)90772-5 · Cited by 217 · see citing works
Popkin, M. K. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800250078010 · Cited by 217 · see citing works
Popov, V. I., & Bocharova, L. S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90337-2 · Cited by 203 · see citing works
Quantitative ultrastructure of Ia boutons in the ventral horn: scaling and positional relationships
Pierce, J., & Mendell, L. M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-11-04748.1993 · Cited by 174 · see citing works
Magariños, A. M., Orchinik, M., & McEwen, B. S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00882-8 · Cited by 163 · see citing works
Self-citationHow Does the Brain Organize Memories?
Eichenbaum, H. (1997) · Science · doi:10.1126/science.277.5324.330 · Cited by 162 · see citing works
Karten, Y. J. G., Nair, S. M., van Essen, L., Sibug, R. M., & Joëls, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13456 · Cited by 150 · see citing works
Lnenicka, G., Atwood, H., & Marin, L. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-08-02252.1986 · Cited by 146 · see citing works
Elliott, E. M., Mattson, M. P., Vanderklish, P., Lynch, G., Chang, I. I., & Sapolsky, R. M. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03537.x · Cited by 136 · see citing works
Differential effects of chronic stress on memory processes in the tree shrew
Ohl, F., & Fuchs, E. (1999) · Cognitive Brain Research · doi:10.1016/s0926-6410(98)00042-1 · Cited by 128 · see citing works
The ‘single’ section Golgi-impregnation procedure: methodological description
Gabbott, P. L. A., & Somogyi, J. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90084-0 · Cited by 127 · see citing works
Stress hormones and brain aging: adding injury to insult?
Porter, N. M., & Landfield, P. W. (1998) · Nature Neuroscience · doi:10.1038/196 · Cited by 119 · see citing works
SCRIBNER, K. A., WALKER, C.-D., CASCIO, C. S., & DALLMAN, M. F. (1991) · Endocrinology · doi:10.1210/endo-129-1-99 · Cited by 112 · see citing works
Renger, J. J., Ueda, A., Atwood, H. L., Govind, C. K., & Wu, C. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-03980.2000 · Cited by 87 · see citing works
Psychiatric Aspects of Diabetes Mellitus
Surridge, D., Erdahl, D. L. W., Lawson, J. S., Donald, M. W., Monga, T. N., BIRD, C. E., & Letemendia, F. J. J. (1984) · The British Journal of Psychiatry · doi:10.1192/bjp.145.3.269 · Cited by 85 · see citing works
Stress and Cardiovascular Disease
Björntorp, P. (2011) · Springer eBooks · doi:10.1007/978-1-84882-419-5 · Cited by 78 · see citing works
Nestler, E. J., Rainbow, T. C., McEwen, B. S., & Greengard, P. (1981) · Science · doi:10.1126/science.6785886 · Cited by 76 · see citing works
Self-citationBrain Uptake of Glucose in Diabetes Mellitus: The Role of Glucose Transporters
Mooradian, A. D., & Morin, A. M. (1991) · The American Journal of the Medical Sciences · doi:10.1097/00000441-199103000-00004 · Cited by 74 · see citing works
Mitochondrial Form and Function Relationships in Vivo: Their Potential in Toxicology and Pathology
Smith, R. A., & Ord, M. J. (1983) · International review of cytology · doi:10.1016/s0074-7696(08)61686-1 · Cited by 67 · see citing works
Bhargava, A., Meijer, O. C., Dallman, M. F., & Pearce, D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03129.2000 · Cited by 58 · see citing works
Stress adaptation and hypersensitivity in 5-HT neuronal systems after repeated foot shock
Ohi, K., Mikuni, M., & Takahashi, K. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90566-2 · Cited by 57 · see citing works
Stress, predisposition and the onset of serious disease: Implications about psychosomatic etiology
Natelson, B. H. (1983) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(83)90031-3 · Cited by 56 · see citing works
Regulation of GLUT-3 glucose transporter in the hippocampus of diabetic rats subjected to stress
Reagan, L. P., Magariños, A. M., Lucas, L., Bueren, A. M. V., McCall, A. L., & McEwen, B. S. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.276.5.e879 · Cited by 56 · see citing works
Self-citationScribner, K. A., Akana, S. F., Walker, C. D., & Dallman, M. F. (1993) · Endocrinology · doi:10.1210/endo.133.6.8243290 · Cited by 50 · see citing works
Circadian rhythm of corticosterone in diabetic rats
Oster, M. H., Castonguay, T. W., Keen, C. L., & Stern, J. S. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90536-x · Cited by 46 · see citing works
The functional significance of biochemical alterations in streptozotocin-induced diabetes
Bellush, L. L., Reid, S. G., & North, D. L. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90424-m · Cited by 43 · see citing works
Diabetes induced by streptozotocin causes reduced Na?K ATPase in the brain
Leong, S. F., & LEUNG, T. K. C. (1991) · Neurochemical Research · doi:10.1007/bf00966596 · Cited by 41 · see citing works
Bellush, L. L., & Rowland, N. E. (1989) · Behavioral Neuroscience · doi:10.1037//0735-7044.103.1.144 · Cited by 41 · see citing works
Avoidance responding in mice with diabetes mellitus
Leedom, L. J., Meehan, W. P., & Zeidler, A. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90029-1 · Cited by 41 · see citing works
Bellush, L. L., & Rowland, N. E. (1989) · Behavioral Neuroscience · doi:10.1037/0735-7044.103.1.144 · Cited by 34 · see citing works
Würzburger, M. I., Prelević, G. M., Sönksen, P. H., PERIC, L. A., Till, S. J., & Morris, R. W. (1990) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1990.tb00926.x · Cited by 32 · see citing works
Hippocampal slices from long-term streptozotocin-injected rats are prone to epileptiform responses
Margineanu, D. G., Niespodziany, I., & Wülfert, E. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00580-1 · Cited by 28 · see citing works
Stress and immune function in diabetes mellitus
Linn, M. W., Linn, B. S., Skyler, J. S., & Jensen, J. A. (1983) · Clinical Immunology and Immunopathology · doi:10.1016/0090-1229(83)90072-7 · Cited by 23 · see citing works
Twenty-four-hour Cortisol Profiles Demonstrate Exaggerated Nocturnal Rise in Diabetic Children
Lebinger, T. G., Saenger, P. H., Fukushima, D. K., Kream, J., Wu, R., & Finkelstein, J. W. (1983) · Diabetes Care · doi:10.2337/diacare.6.5.506 · Cited by 21 · see citing works
Flagged first, then by citations
Research works printed but not linked: 6
- [4]McEwen B S, Stellar E. Arch Int Med. 1993;153:2093–2101. [PubMed] [Google Scholar]
- [11]Lupien S J, de Leon M, de Santi S, Convit A, Tarshish C, Nair N P, Thakur M, McEwen B S, Hauger R L, Meaney M J. Nat Neurosci. 1998;1:3–4. [Google Scholar]
- [20]Bjorntorp P. Acta Physiol Scand. 1997;640:144–148. [PubMed] [Google Scholar]
- [23]Rerup C. Pharmacol Rev. 1970;22:485–518. [PubMed] [Google Scholar]
- [34]De Nicola A F, Magariños A M, Foglia V G. In: Diabetes. Rifkin H, Colwell J A, Taylor S I, editors. Amsterdam: Elsevier; 1991. pp. 3–7. [Google Scholar]
- [59]Partridge W M, Castonguay T M, Keen Cl, Stern J S. Life Sci. 1988;43:1643–1645. doi: 10.1016/0024-3205(88)90536-x. [DOI] [PubMed] [Google Scholar] · DOI
Cited by
Sorted by citations
McEwen, B. S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02950-4 · Cited by 1,827 · see citing works
Self-citationSynaptic plasticity and depression: new insights from stress and rapid-acting antidepressants
Duman, R. S., Aghajanian, G. K., Sanacora, G., & Krystal, J. H. (2016) · Nature Medicine · doi:10.1038/nm.4050 · Cited by 1,750 · see citing works
Intranasal insulin improves memory in humans
Benedict, C., Hallschmid, M., Hatke, A., Schultes, B., Fehm, H. L., Born, J., & Kern, W. (2004) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.04.003 · Cited by 699 · see citing works
Stranahan, A. M., Arumugam, T. V., Cutler, R. G., Lee, K. M., Egan, J. M., & Mattson, M. P. (2008) · Nature Neuroscience · doi:10.1038/nn2055 · Cited by 610 · see citing works
Allostasis and the human brain: Integrating models of stress from the social and life sciences
Ganzel, B., Morris, P. A., & Wethington, E. (2010) · Psychology Review · doi:10.1037/a0017773 · Cited by 370 · see citing works
Glucose transporter expression in the central nervous system: relationship to synaptic function
McEwen, B. S., & Reagan, L. P. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.041 · Cited by 378 · see citing works
Self-citationConvit, A., Wolf, O. T., Tarshish, C., & de Leon, M. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0336073100 · Cited by 347 · see citing works
Arnold, S. E., Lucki, I., Brookshire, B. R., Carlson, G. C., Browne, C. A., Kazi, H., Bang, S., Choi, B., Chen, Y., McMullen, M. F., et al. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.03.011 · Cited by 315 · see citing works
Enhanced Risk for Alzheimer Disease in Persons With Type 2 Diabetes and APOE ε4
Irie, F., Fitzpatrick, A. L., López, O. L., Kuller, L. H., Peila, R., Newman, A. B., & Launer, L. J. (2008) · Archives of Neurology · doi:10.1001/archneurol.2007.29 · Cited by 304 · see citing works
Micheli, L., Ceccarelli, M., D’Andrea, G., & Tirone, F. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.09.002 · Cited by 288 · see citing works
Jolivalt, C. G., Lee, C. A., Beiswenger, K., Smith, J., Orlov, M., Torrance, M., & Masliah, E. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21787 · Cited by 281 · see citing works
Effects of diabetes on hippocampal neurogenesis: Links to cognition and depression
Ho, N., Sommers, M. S., & Lucki, I. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.03.010 · Cited by 271 · see citing works
Chronic stress, metabolism, and metabolic syndrome
Tamashiro, K. L., Sakai, R. R., Shively, C. A., Karatsoreos, I. N., & Reagan, L. P. (2011) · Stress · doi:10.3109/10253890.2011.606341 · Cited by 222 · see citing works
Flores, G., Alquicer, G., Gómez, A. B. S., Zaldivar, G. A., Stewart, J., Quirion, R., & Srivastava, L. K. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.02.021 · Cited by 220 · see citing works
Neuronal Apoptosis in Neurodegeneration
Okouchi, M., Ekshyyan, O. Y., Maracine, M., & Aw, T. Y. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1511 · Cited by 219 · see citing works
Crochemore, C., Lu, J., Wu, Y., Liposits, Z., Sousa, N., Holsboer, F., & Almeida, O. F. X. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001679 · Cited by 210 · see citing works
McIntyre, R. S., Soczynska, J. K., Konarski, J. Z., & Kennedy, S. H. (2005) · Expert Opinion on Drug Safety · doi:10.1517/14740338.5.1.157 · Cited by 200 · see citing works
A look inside the diabetic brain: Contributors to diabetes-induced brain aging
Wrighten, S. A., Piroli, G. G., Grillo, C. A., & Reagan, L. P. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.10.013 · Cited by 195 · see citing works
Type 2 diabetes and risk of cognitive impairment and dementia
Whitmer, R. A. (2007) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-007-0058-7 · Cited by 195 · see citing works
de Kloet, E. R., DeRijk, R. H., & Meijer, O. C. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0403 · Cited by 193 · see citing works
Chornenkyy, Y., Wang, W., Wei, A. L., & Nelson, P. T. (2018) · Brain Pathology · doi:10.1111/bpa.12655 · Cited by 184 · see citing works
Hippocampal synaptic plasticity and glutamate receptor regulation: influences of diabetes mellitus.
Trudeau, F., Gagnon, S., & Massicotte, G. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.055 · Cited by 187 · see citing works
Inside the Diabetic Brain: Role of Different Players Involved in Cognitive Decline
Gaspar, J. M., Baptista, F. I., Macedo, M. P., & Ambrósio, A. F. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00240 · Cited by 179 · see citing works
Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress
Chen, Y., Brunson, K. L., Adelmann, G., Bender, R. A., Frotscher, M., & Baram, T. Z. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.03.036 · Cited by 179 · see citing works
Leptin neuroprotection in the CNS: mechanisms and therapeutic potentials
Signore, A. P., Zhang, F., Weng, Z., Gao, Y., & Chen, J. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05457.x · Cited by 152 · see citing works
Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats
Zhang, W.-J., Tan, Y., Yue, J. T. Y., Vranić, M., & Wojtowicz, J. M. (2007) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.2007.00928.x · Cited by 150 · see citing works
The brain in diabetes: molecular changes in neurons and their implications for end-organ damage
Klein, J. P., & Waxman, S. G. (2003) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00503-9 · Cited by 131 · see citing works
Cognitive dysfunction and hippocampal changes in experimental type 1 diabetes
Alvarez, E. O., Beauquis, J., Revsin, Y., Banzán, A. M., Roig, P., Nicola, A. F. D., & Saravia, F. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.001 · Cited by 130 · see citing works
Beauquis, J., Roig, P., Nicola, A. F. D., & Saravia, F. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013993 · Cited by 129 · see citing works
Beauquis, J., Roig, P., Homo‐Delarche, F., Nicola, A. F. D., & Saravia, F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04691.x · Cited by 128 · see citing works
Saravia, F., Revsin, Y., Deniselle, M. C. G., González, S. L., Roig, P., Lima, A. E., Homo‐Delarche, F., & Nicola, A. F. D. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03675-2 · Cited by 124 · see citing works
Hernández-Fonseca, J. P., Rincon, J. C., Pedreáñez, A. B., Viera, N., Arcaya, J. L., Carrizo, E., & Mosquera, J. (2009) · Experimental Diabetes Research · doi:10.1155/2009/329632 · Cited by 123 · see citing works
Studies of hormone action in the hippocampal formation
McEwen, B. S., Magariños, A. M., & Reagan, L. P. (2002) · Journal of Psychosomatic Research · doi:10.1016/s0022-3999(02)00307-0 · Cited by 123 · see citing works
Self-citationMartínez‐Téllez, R. I., Gómez-Villalobos, M. D. J., & Flores, G. (2005) · Brain Research · doi:10.1016/j.brainres.2005.04.048 · Cited by 121 · see citing works
Revsin, Y., Rekers, N. V., Louwe, M. C., Saravia, F. E., De Nicola, A. F., de Kloet, E. R., & Oitzl, M. S. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.136 · Cited by 119 · see citing works
Insulin signaling effects on memory and mood
Reagan, L. P. (2007) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.10.012 · Cited by 118 · see citing works
Khan, M. S., Misra, S. K., Wang, Z., Daza, E., Schwartz‐Duval, A. S., Kus, J., Pan, D., & Pan, D. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.6b04769 · Cited by 117 · see citing works
The As and Ds of stress: Metabolic, morphological and behavioral consequences
Reagan, L. P., Grillo, C. A., & Piroli, G. G. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.02.050 · Cited by 111 · see citing works
Diabetes and cognitive function: An evidence-based current perspective
Sebastian, M. J., Khan, S. K. A., Pappachan, J. M., & Jeeyavudeen, M. S. (2023) · World Journal of Diabetes · doi:10.4239/wjd.v14.i2.92 · Cited by 111 · see citing works
Interactions Between Age, Stress and Insulin on Cognition: Implications for Alzheimer's Disease
Solas, M., Aisa, B., Mugueta, M. C., Del Río, J., Tordera, R. M., & Ramírez, M. J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.13 · Cited by 124 · see citing works
Structural plasticity and tianeptine: cellular and molecular targets
McEwen, B. S., Magarinos, A. M., & Reagan, L. P. (2002) · European Psychiatry · doi:10.1016/s0924-9338(02)00650-8 · Cited by 108 · see citing works
Self-citationGrillo, C. A., Piroli, G. G., Wood, G. E., Reznikov, L. R., McEwen, B. S., & Reagan, L. P. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.019 · Cited by 106 · see citing works
Self-citationReagan, L. P., Gorovits, N., Hoskin, E. K., Alves, S. E., Katz, E. B., Grillo, C. A., Piroli, G. G., McEwen, B. S., & Charron, M. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051629798 · Cited by 106 · see citing works
Self-citationVanGuilder, H. D., Brucklacher, R. M., Patel, K. M., Ellis, R. W., Freeman, W. M., & Barber, A. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06322.x · Cited by 103 · see citing works
Cognitive dysfunction associated with metabolic syndrome
Taylor, V. H., & MacQUEEN, G. M. (2007) · Obesity Reviews · doi:10.1111/j.1467-789x.2007.00401.x · Cited by 102 · see citing works
Models and mechanisms for hippocampal dysfunction in obesity and diabetes
Stranahan, A. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.045 · Cited by 101 · see citing works
Diabetes as a chronic metabolic stressor: Causes, consequences and clinical complications
Reagan, L. P. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.02.004 · Cited by 101 · see citing works
Neuronal and astroglial alterations in the hippocampus of a mouse model for type 1 diabetes
Revsin, Y., Saravia, F., Roig, P., Lima, A. E., de Kloet, E. R., Homo‐Delarche, F., & Nicola, A. F. D. (2005) · Brain Research · doi:10.1016/j.brainres.2004.12.032 · Cited by 97 · see citing works
Chiroma, S. M., Baharuldin, M. T. H., Taib, C. N. M., Amom, Z., Jagadeesan, S., Adenan, M. I., & Moklas, M. A. M. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.10.111 · Cited by 96 · see citing works
Piroli, G. G., Grillo, C. A., Hoskin, E. K., Znamensky, V., Katz, E. B., Milner, T. A., McEwen, B. S., Charron, M. J., & Reagan, L. P. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10368 · Cited by 95 · see citing works
Self-citationCeretta, L. B., Réus, G. Z., Abelaira, H. M., Ribeiro, K. F., Zappellini, G., Felisbino, F. F., Steckert, A. V., Dal‐Pizzol, F., & Quevedo, J. (2012) · Experimental Diabetes Research · doi:10.1155/2012/302682 · Cited by 94 · see citing works
Sousa, V. C., Vital, J., Costenla, A. R., Batalha, V. L., Sebastião, A. M., Ribeiro, J. A., & Lopes, L. V. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.01.024 · Cited by 94 · see citing works
Saravia, F., Revsin, Y., Lux-Lantos, V. A., Beauquis, J., Homo-Delarche, F., & Nicola, A. F. D. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01223.x · Cited by 91 · see citing works
Diabetes and brain aging: Epidemiologic evidence
Launer, L. J. (2005) · Current Diabetes Reports · doi:10.1007/s11892-005-0069-1 · Cited by 85 · see citing works
Bomba, M., Ciavardelli, D., Silvestri, E., Canzoniero, L. M. T., Lattanzio, R., Chiappini, P. B. O., Piantelli, M., Ilio, C. D., Consoli, A., & Sensi, S. L. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.139 · Cited by 84 · see citing works
Brain glucose metabolism in an animal model of depression
Detka, J., Kurek, A., Kucharczyk, M. W., Głombik, K., Basta‐Kaim, A., Kubera, M., Lasoń, W., & Budziszewska, B. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.046 · Cited by 82 · see citing works
Calvo‐Ochoa, E., & Arias, C. (2014) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2531 · Cited by 80 · see citing works
Neuroendocrine link between stress, depression and diabetes
Detka, J., Kurek, A., Basta‐Kaim, A., Kubera, M., Lasoń, W., & Budziszewska, B. (2013) · Pharmacological Reports · doi:10.1016/s1734-1140(13)71520-2 · Cited by 77 · see citing works
Tanokashira, D., Kurata, E., Fukuokaya, W., Kawabe, K., Mana, K., Takeuchi, H., Nakazato, M., & Taguchi, A. (2018) · FEBS Open Bio · doi:10.1002/2211-5463.12436 · Cited by 76 · see citing works
Asiaticoside attenuates diabetes-induced cognition deficits by regulating PI3K/Akt/NF-κB pathway
Yin, Z., Yu, H., Chen, S., Ma, C., Ma, X., Xu, L., Ma, Z., Qu, R., & Ma, S. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.06.024 · Cited by 75 · see citing works
Brain Endothelial Cells Control Fertility through Ovarian-Steroid–Dependent Release of Semaphorin 3A
Giacobini, P., Parkash, J., Campagne, C., Messina, A., Casoni, F., Vanacker, C., Langlet, F., Hobo, B., Cagnoni, G., Gallet, S., et al. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001808 · Cited by 74 · see citing works
Grillo, C. A., Piroli, G. G., Rosell, D. R., Hoskin, E. K., Mcewen, B. S., & Reagan, L. P. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00343-9 · Cited by 73 · see citing works
Self-citationHippocampal Neuropathology of Diabetes Mellitus is Relieved by Estrogen Treatment
Saravia, F., Beauquis, J., Revsin, Y., Homo‐Delarche, F., de Kloet, E. R., & Nicola, A. F. D. (2006) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9096-y · Cited by 72 · see citing works
Soares, L. M., Vry, J. D., Steinbusch, H. W. M., Milani, H., Prickaerts, J., & de Oliveira, R. M. W. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.062 · Cited by 70 · see citing works
Physiological and Pathophysiological Implications of Synaptic Tau
Regan, P. L., Whitcomb, D. J., & Cho, K. (2016) · The Neuroscientist · doi:10.1177/1073858416633439 · Cited by 70 · see citing works
Hemmati, A. A., Alboghobeish, S., & Ahangarpour, A. (2018) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2018.22.3.257 · Cited by 69 · see citing works
Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice
Saravia, F., Beauquis, J., Pietranera, L., & Nicola, A. F. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.012 · Cited by 67 · see citing works
Sharma, S. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2021.113528 · Cited by 65 · see citing works
Beauquis, J., Homo‐Delarche, F., Giroix, M.-H., Ehses, J. A., Coulaud, J., Roig, P., Portha, B., Nicola, A. F. D., & Saravia, F. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2009.12.022 · Cited by 64 · see citing works
Diabetes-associated depression: The serotonergic system as a novel multifunctional target
Gupta, D., Prabhakar, V., Kanade, P., & Radhakrishnan, M. (2015) · Indian Journal of Pharmacology · doi:10.4103/0253-7613.150305 · Cited by 64 · see citing works
Lechuga-Sancho, A. M., Arroba, A. I., Frago, L. M., García-Cáceres, C., de Célix, A. D.-R., Argente, J., & Chowen, J. A. (2006) · Endocrinology · doi:10.1210/en.2006-0766 · Cited by 64 · see citing works
Insulin dysfunction and allostatic load in bipolar disorder
Brietzke, E. M., Kapczinski, F. P., Grassi‐Oliveira, R., Grande, I., Vieta, E., & McIntyre, R. S. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.10.185 · Cited by 64 · see citing works
Calaza, K. D. C., Martinez, A. B., Mendonça, H. R., & Carpi-Santos, R. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.266910 · Cited by 64 · see citing works
Impact of Energy Intake and Expenditure on Neuronal Plasticity
Stranahan, A. M., & Mattson, M. P. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8043-0 · Cited by 63 · see citing works
Khan, M. S., Dighe, K., Wang, Z., Srivastava, I., Schwartz‐Duval, A. S., Misra, S. K., & Pan, D. (2018) · The Analyst · doi:10.1039/c8an02085j · Cited by 63 · see citing works
Yi, S. S., Hwang, I. K., Yoo, K., Park, O. K., Yu, J., Yan, B., Kim, I. Y., Kim, Y. N., Pai, T.-K., Song, W. J., et al. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9870-y · Cited by 62 · see citing works
Aerobic Physical Exercise as a Possible Treatment for Neurocognitive Dysfunction in Bipolar Disorder
Kucyi, A., Alsuwaidan, M. T., Liauw, S. S. L., & McIntyre, R. S. (2010) · Postgraduate Medicine · doi:10.3810/pgm.2010.11.2228 · Cited by 62 · see citing works
Guo, J., Yu, C., Li, H., Liu, F., Feng, R., Wang, H., Meng, Y., Li, Z., Ju, G., & Wang, J. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.08.012 · Cited by 57 · see citing works
Neuronal insulin signal transduction mechanisms in diabetes phenotypes
Reagan, L. P. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.09.001 · Cited by 56 · see citing works
Dobretsov, M. G., Hastings, S. L., Stimers, J. R., & Zhang, J.-M. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(01)00410-1 · Cited by 56 · see citing works
Glucose, stress, and hippocampal neuronal vulnerability
Reagan, L. P. (2002) · International review of neurobiology · doi:10.1016/s0074-7742(02)51009-6 · Cited by 55 · see citing works
Gaspar, J. M., Baptista, F. I., Galvão, J., Castilho, Á., Cunha, R. A., & Ambrósio, A. F. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.021 · Cited by 53 · see citing works
Saliva Lab-on-a-chip biosensors: Recent novel ideas and applications in disease detection
Mohammadi, M. H., Mulder, S. E., Khashayar, P., Kalbasi, A., Azimzadeh, M., & Aref, A. R. (2021) · Microchemical Journal · doi:10.1016/j.microc.2021.106506 · Cited by 52 · see citing works
Weeks, J. C. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00102-3 · Cited by 52 · see citing works
Diabetes type II: A risk factor for depression-Parkinson–Alzheimer?
Riederer, P., Bartl, J., Laux, G., & Grünblatt, E. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9203-1 · Cited by 51 · see citing works
de la Vega, E. G., Gómez‐Villalobos, M. D. J., & Flores, G. (2004) · Brain Research · doi:10.1016/j.brainres.2004.06.042 · Cited by 51 · see citing works
Relationship between regional brain metabolism, illness severity and age in depressed subjects
Konarski, J. Z., Kennedy, S. H., McIntyre, R. S., Rafi‐Tari, S., Soczynska, J. K., & Mayberg, H. S. (2007) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.02.001 · Cited by 50 · see citing works
Elevated Brain Glucose and Glycogen Concentrations in an Animal Model of Depression
Detka, J., Kurek, A., Basta‐Kaim, A., Kubera, M., Lasoń, W., & Budziszewska, B. (2014) · Neuroendocrinology · doi:10.1159/000368607 · Cited by 50 · see citing works
Downregulation of LPR1 at the blood–brain barrier in streptozotocin-induced diabetic mice
Hong, H., Liu, L. P., Liao, J. M., Wang, T. S., Ye, F.-Y., Wu, J., Wang, Y. Y., Wang, Y., Li, Y. Q., & Long, Y. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.03.001 · Cited by 50 · see citing works
Pietranera, L., Saravia, F., Deniselle, M. C. G., Roig, P., Lima, A. E., & Nicola, A. F. D. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01436.x · Cited by 49 · see citing works
Piroli, G. G., Grillo, C. A., Charron, M. J., McEwen, B. S., & Reagan, L. P. (2004) · Brain Research · doi:10.1016/j.brainres.2004.01.044 · Cited by 49 · see citing works
Self-citationOkouchi, M., Okayama, N., & Aw, T. Y. (2005) · Current Neurovascular Research · doi:10.2174/1567202052773535 · Cited by 48 · see citing works
Altar, C. A., Hunt, R. A., Jurata, L. W., Webster, M. J., Derby, E. G., Gallagher, P., Lemire, A. L., Brockman, J. A., & Laeng, P. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.08.031 · Cited by 48 · see citing works
Accelerated cognitive aging in diabetic rats is prevented by lowering corticosterone levels
Stranahan, A. M., Lee, K. M., Pistell, P. J., Nelson, C. M., Readal, N., Miller, M. G., Spangler, E. L., Ingram, D. K., & Mattson, M. P. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.05.005 · Cited by 48 · see citing works
Maghami, S., Zardooz, H., Khodagholi, F., Binayi, F., Saber, R. R., Hedayati, M., Sahraei, M., & Ansari, M. A. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204731 · Cited by 47 · see citing works
Reagan, L. P., & McEwen, B. S. (2002) · Neuroreport · doi:10.1097/00001756-200210070-00022 · Cited by 47 · see citing works
Self-citationDiabetes and neurodegeneration in the brain
Toth, C. C. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53480-4.00035-7 · Cited by 46 · see citing works
Hippocampal calcium dysregulation at the nexus of diabetes and brain aging
Thibault, O., Anderson, K. L., DeMoll, C., Brewer, L. D., Landfield, P. W., & Porter, N. M. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.07.024 · Cited by 45 · see citing works
Upregulation of RAGE at the blood‐brain barrier in streptozotocin‐induced diabetic mice
Liu, L. P., Hong, H., Liao, J. M., Wang, T. S., Wu, J., Chen, S. S., Li, Y. Q., Long, Y., & Xia, Y. Z. (2009) · Synapse · doi:10.1002/syn.20644 · Cited by 44 · see citing works
Yang, H., Fan, S.-R., Song, D.-P., Wang, Z., Ma, S., Li, S., Li, X., Xu, M., Xu, M., & Wang, X. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2012.1227 · Cited by 44 · see citing works
- Authors
- Magariños, A. M., & McEwen, B. S.
- Affiliations
- The Rockefeller University, 1230 York Avenue, New York, NY 10021
- Rockefeller University (US)
- ORCID
- McEwen, Bruce S.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2000-09-26
- Volume
- 97
- Issue
- 20
- Pages
- 11056-11061
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC27147
- OpenAlex
- W2116721266
- Cited by
- 262
- References
- 62
- Citations by year
- 2026: 3 · 2024: 7 · 2023: 6 · 2022: 6 · 2021: 5 · 2020: 8 · 2019: 8 · 2018: 15 · 2017: 9 · 2016: 11 · 2015: 18 · 2014: 13 · 2013: 17 · 2012: 13
- FWCI
- 2.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-41256, R37MH041256, R01MH041256)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- experimental diabetes, streptozotocin-induced diabetes, hippocampus, CA3 pyramidal cells, dendritic reorganization, mossy fiber terminals, synaptic vesicle depletion, chronic stress, restraint stress, corticosterone, adrenal hypertrophy, glucocorticoid secretion, hippocampal synaptic plasticity
- MeSH terms
- Animals, Anti-Bacterial Agents, Corticosterone, Dendrites, Diabetes Mellitus, Experimental, Hippocampus, Male, Streptozocin, Stress, Physiological, Synapses, Rats, Sprague-Dawley, 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