Cited by 141Traumatic Brain Injury and Neurovascular DisturbancesTraumatic Brain Injury ResearchAutomotive and Human Injury Biomechanics

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Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury

Wagner, Amy K., Willard, Lauren A., Kline, Anthony E., Wenger, Michael K., Bolinger, Bryan D., Ren, Dianxu, Zafonte, Ross D., Dixon, C.Edward·2004·Brain Research

DOI 10.1016/j.brainres.2003.11.027

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Abstract

Female sex hormones are acutely neuroprotective in experimental models of traumatic brain injury (TBI). Because hormonal profiles are known to vary with estrous cycle stage, the purpose of this study was to evaluate how pre-injury estrous stage affects motor and cognitive performance after experimental TBI. We also sought to compare post-injury behavioral performance in males vs. females. Under anesthesia, male (n=18) and female (n=35) Sprague-Dawley rats underwent either controlled cortical impact (CCI) injury (2.7 mm; 4 m/s) or sham operations. Females were grouped according to estrous stage (proestrous or non-proestrous) at the time of surgery. Motor function was assessed pre-injury and for the first 5 days after surgery using beam balance and walking tasks. Spatial memory was assessed beginning 14 days post-injury utilizing the Morris water maze (MWM) task. No significant differences were found on any task between injured females regardless of estrous cycle stage. Females performed significantly better than males on both motor tasks, but gender did not influence MWM performance. Mixed effects multivariate analysis corroborated these results by showing that pre-injury serum hormone levels had little affect on behavioral performance. The results suggest that the presence of endogenous circulating hormones, rather than hormonal status at time of injury, may confer early neuroprotection in females after TBI. The impact of early neuroprotection on later behavioral outcome and the anatomic structural specificity of hormonal neuroprotection require further study.

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Plasma Concentration of LH, FSH, Prolactin, Progesterone and Estradiol-17β Throughout the 4-Day Estrous Cycle of the Rat
Butcher, R. L., COLLINS, W. E., & FUGO, N. W. (1974) · Endocrinology · doi:10.1210/endo-94-6-1704 · Cited by 1,313
A controlled cortical impact model of traumatic brain injury in the rat
Edward Dixon, C., Clifton, G. L., Lighthall, J. W., Yaghmai, A. A., & Hayes, R. L. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90104-8 · Cited by 1,141
Amphetamine, Haloperidol, and Experience Interact to Affect Rate of Recovery After Motor Cortex Injury
Feeney, D. M., Gonzalez, A., & Law, W. A. (1982) · Science · doi:10.1126/science.7100929 · Cited by 921
Gender Differences in Acute CNS Trauma and Stroke: Neuroprotective Effects of Estrogen and Progesterone
Roof, R. L., & Hall, E. D. (2000) · Journal of Neurotrauma · doi:10.1089/neu.2000.17.367 · Cited by 652
17-β Estradiol Protects Neurons from Oxidative Stress-Induced Cell Death in Vitro
Behl, C., Widmann, M., Trapp, T., & Holsboer, F. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2647 · Cited by 608
Estrogen receptor α, not β, is a critical link in estradiol-mediated protection against brain injury
Dubal, D. B., Zhu, H., Yu, J., Rau, S. W., Shughrue, P. J., Merchenthaler, I. J., Kindy, M. S., & Wise, P. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.4.1952 · Cited by 550
Oestrogen as a neuroprotective hormone
Behl, C. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn846 · Cited by 489
Do women fare worse: a metaanalysis of gender differences in traumatic brain injury outcome
Farace, E., & Alves, W. M. (2000) · Journal of neurosurgery · doi:10.3171/jns.2000.93.4.0539 · Cited by 446
Spatial and nonspatial learning across the rat estrous cycle.
Warren, S. G., & Juraska, J. M. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.2.259 · Cited by 424
Estrogen as a Neuroprotectant in Stroke
Hurn, P. D., & Macrae, I. M. (2000) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200004000-00001 · Cited by 401
Cognitive Deficits Following Traumatic Brain Injury Produced by Controlled Cortical Impact
Hamm, R. J., Dixon, C. E., White-Gbadebo, D. M., Singha, A. K., Jenkins, L. W., Lyeth, B. G., & HAYES, R. L. (1992) · Journal of Neurotrauma · doi:10.1089/neu.1992.9.11 · Cited by 344
Self-citation
Spatial and nonspatial learning across the rat estrous cycle.
Warren, S. G., & Juraska, J. M. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.2.259 · Cited by 341
Gender influences outcome of brain injury: progesterone plays a protective role
Roof, R. L., Duvdevani, R., & Stein, D. G. (1993) · Brain Research · doi:10.1016/0006-8993(93)91526-x · Cited by 327
Progesterone Facilitates Cognitive Recovery and Reduces Secondary Neuronal Loss Caused by Cortical Contusion Injury in Male Rats
Roof, R. L., Duvdevani, R., Braswell, L., & Stein, D. G. (1994) · Experimental Neurology · doi:10.1006/exnr.1994.1147 · Cited by 322
Progesterone protects against lipid peroxidation following traumatic brain injury in rats
Roof, R. L., Hoffman, S. W., & Stein, D. G. (1997) · Molecular and Chemical Neuropathology · doi:10.1007/bf02815156 · Cited by 316
One-Year Study of Spatial Memory Performance, Brain Morphology, and Cholinergic Markers After Moderate Controlled Cortical Impact in Rats
Dixon, C. E., Kochanek, P. M., Yan, H. Q., Schiding, J. K., GRIFFITH, R. G., Baum, E., Marion, D. W., & DeKosky, S. T. (1999) · Journal of Neurotrauma · doi:10.1089/neu.1999.16.109 · Cited by 303
Self-citation
Estradiol upregulates Bcl-2 expression in adult brain neurons
García‐Segura, L. M., Cardona‐Gómez, G. P., Naftolin, F. N., & Chowen, J. A. (1998) · Neuroreport · doi:10.1097/00001756-199803090-00006 · Cited by 253
Disruption of estrogen receptor β gene impairs spatial learning in female mice
Rissman, E. F., Heck, A. L., Leonard, J. E., Shupnik, M. A., & Gustafsson, J.-Α. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012032699 · Cited by 245
Estrogen-Related Gender Difference in Survival Rate and Cortical Blood Flow After Impact-Acceleration Head Injury in Rats
Roof, R. L., & Hall, E. D. (2000) · Journal of Neurotrauma · doi:10.1089/neu.2000.17.1155 · Cited by 233
Neuropathological Protection after Traumatic Brain Injury in Intact Female Rats Versus Males or Ovariectomized Females
Bramlett, H. M., & Dietrich, W. D. (2001) · Journal of Neurotrauma · doi:10.1089/089771501750451811 · Cited by 213
Spatial learning and memory at defined points of the estrous cycle: Effects on performance of a hippocampal-dependent task.
Berry, B. J. L., McMahan, R., & Gallagher, M. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.2.267 · Cited by 212
Severe controlled cortical impact in rats: assessment of cerebral edema, blood flow, and contusion volume
KOCHANEK, P. M., MARION, D. W., ZHANG, W., SCHIDING, J. K., WHITE, M., PALMER, A. M., CLARK, R. S. B., O'MALLEY, M. E., STYREN, S. D., HO, C., et al. (1995) · Journal of Neurotrauma · doi:10.1089/neu.1995.12.1015 · Cited by 203
Time course of oxidative damage in different brain regions following transient cerebral ischemia in gerbils
Candelario‐Jalil, E., Mhadu, N. H., Al-Dalain, S. M., Martı́nez, G., & León, O. S. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(01)00282-6 · Cited by 194
Female sex steroid hormones: from receptors to networks to performance—actions on the sensorimotor system
Smith, S. S. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90057-4 · Cited by 178
Spatial learning and memory at defined points of the estrous cycle: Effects on performance of a hippocampal-dependent task.
Berry, B. J. L., McMahan, R., & Gallagher, M. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.2.267 · Cited by 175
The laboratory rat
Sharp, P. E., & Villano, J. (2013) · Cited by 165
Attenuation of Working Memory and Spatial Acquisition Deficits after a Delayed and Chronic Bromocriptine Treatment Regimen in Rats Subjected to Traumatic Brain Injury by Controlled Cortical Impact
Kline, A. E., Massucci, J. L., Marion, D. W., & Dixon, C. E. (2002) · Journal of Neurotrauma · doi:10.1089/08977150252932370 · Cited by 147
Self-citation
Cognitive Impairment Following Closed Head Injury
Capruso, D. X., & Levin, H. S. (1992) · Neurologic Clinics · doi:10.1016/s0733-8619(18)30185-3 · Cited by 147
Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea.
Williams, N. I., Caston-Balderrama, A. L., Helmreich, D. L., Parfitt, D., Nosbisch, C., & Cameron, J. L. (2001) · Endocrinology · doi:10.1210/endo.142.6.8113 · Cited by 146
Cerebral vasodilating capacity during forebrain ischemia
Pelligrino, D. A., Santizo, R. A., Baughman, V. L., & Wang, Q. (1998) · Neuroreport · doi:10.1097/00001756-199810050-00026 · Cited by 144
Serum Progesterone Levels Correlate with Decreased Cerebral Edema after Traumatic Brain Injury in Male Rats
Wright, D. W., Bauer, M. E., Hoffman, S. W., & Stein, D. G. (2001) · Journal of Neurotrauma · doi:10.1089/089771501750451820 · Cited by 132
β-Estradiol protects hippocampal CA1 neurons against transient forebrain ischemia in gerbil
Sudo, S., Wen, T., Desaki, J., Matsuda, S., Tanaka, J., Arai, T., Maeda, N., & Sakanaka, M. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(97)00106-5 · Cited by 126
Gender-specific impairment on Morris water maze task after entorhinal cortex lesion
Roof, R. L., Zhang, Q., Glasier, M. M., & Stein, D. G. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90060-4 · Cited by 125
Chronic methylphenidate treatment enhances water maze performance following traumatic brain injury in rats
Kline, A. E., Yan, H. Q., Bao, J., Marion, D. W., & Dixon, C. E. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)00797-7 · Cited by 118
Self-citation
Estrogen Receptor-Mediated Neuroprotection from Oxidative Stress Requires Activation of the Mitogen-Activated Protein Kinase Pathway
Mize, A. L., Shapiro, R. A., & Dorsa, D. M. (2002) · Endocrinology · doi:10.1210/en.2002-220698 · Cited by 118
Spatial working memory in rats: no differences between the sexes
Healy, S. D., Braham, S. R., & Braithwaite, V. A. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0923 · Cited by 115
Sex Differences in the Activational Effect of ERα on Spatial Learning
Fugger, H. N., Cunningham, S. G., Rissman, E. F., & Foster, T. C. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1475 · Cited by 111
Intervention with environmental enrichment after experimental brain trauma enhances cognitive recovery in male but not female rats
Wagner, A. K., Kline, A. E., Sokoloski, J. E., ZAFONTE, R. D., Capulong, E., & Dixon, C. E. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01103-5 · Cited by 104
Self-citation
Estrogen attenuates over-expression of β-amyloid precursor protein messager RNA in an animal model of focal ischemia
Shi, J., Panickar, K. S., Yang, S.-H., Rabbani, O., Day, A. L., & Simpkins, J. W. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00888-9 · Cited by 95
17β-Estradiol reduces cortical lesion size in the glutamate excitotoxicity model by enhancing extracellular lactate: a new neuroprotective pathway
Mendelowitsch, A., Ritz, M., Ros, J., Langemann, H., & Gratzl, O. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02359-9 · Cited by 94
Estrogen prevents the loss of CA1 hippocampal neurons in gerbils after ischemic injury
Shughrue, P. J., & Merchenthaler, I. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00790-x · Cited by 90
Use of Injury Severity Variables in Determining Disability and Community Integration after Traumatic Brain Injury
Wagner, A. K., Hammond, F. M., Sasser, H. C., Wiercisiewski, D. R., & Norton, H. J. (2000) · doi:10.1097/00005373-200009000-00005 · Cited by 87
Self-citation
Deleterious effect of β-estradiol in a rat model of transient forebrain ischemia
Izumi, H., Hurn, P., & Crain, B. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02278-8 · Cited by 85
Head trauma: basic, preclinical, and clinical directions: Edited by Leonard P Miller and Ronald L Hayes (Pp 494, pound107.00). Published by Wiley-Liss, New York, 2001. ISBN 0471 360 155
Kirkpatrick, P. J. (2002) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.72.2.279-b · Cited by 78
Sex-related differences in cortical function after medial frontal lesions in rats.
Kolb, B. E., & Cioe, J. D. D. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.6.1271 · Cited by 71
Sex-related differences in cortical function after medial frontal lesions in rats.
Kolb, B. E., & Cioe, J. D. D. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.6.1271 · Cited by 59
Effects of the duration of progesterone treatment on the resolution of cerebral edema induced by cortical contusions in rats.
Galani, R., Hoffman, S. W., & Stein, D. G. (2001) · PubMed · Cited by 56
Does endogenous progesterone promote recovery of chronic sensorimotor deficits following contusion to the forelimb representation of the sensorimotor cortex?
Grossman, K., & Stein, D. G. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00275-8 · Cited by 31
Untitled work
(1997) · doi:10.1002/(sici)1096-9861(19971201)388:4

Research works printed but not linked: 1

Bryan, 2001, Disruption of the estrous cycle in the female rat following head injury, J. Neurotrauma, 18, 1129

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Authors: Wagner, A. K., Willard, L. A., Kline, A. E., Wenger, M. K., Bolinger, B. D., Ren, D., Zafonte, R. D., & Dixon, C. E.
Affiliations: University of Pittsburgh (US)
Corresponding author: Wagner, Amy K.
ORCID: Wagner, Amy K.
Kline, Anthony E.
Ren, Dianxu
Zafonte, Ross D.
Dixon, C.Edward
Venue: Brain Research
Publisher: Elsevier BV
Published: 2004-02
Volume: 998
Issue: 1
Pages: 113-121
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/j.brainres.2003.11.027
OpenAlex: W2035277900
Cited by: 141
References: 46
Citations by year: 2026: 6 · 2025: 3 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 3 · 2020: 6 · 2019: 10 · 2018: 5 · 2017: 7 · 2016: 7 · 2015: 12 · 2014: 13 · 2013: 6 · 2012: 3
FWCI: 3.23
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (K08HD40833, R03HD41399)
Topics: Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
Physical Sciences › Engineering › Biomedical Engineering › Automotive and Human Injury Biomechanics
Keywords: traumatic brain injury, estrous cycle stage, sex differences, female sex hormones, neuroprotection, motor function, spatial memory, controlled cortical impact, serum hormone levels
MeSH terms: Analysis of Variance, Animals, Brain Injuries, Cognition, Disease Models, Animal, Estrogens, Female, Gender Identity, Male, Motor Activity, Progesterone, Psychomotor Performance, Reaction Time, Time Factors, Vagina, Rats, Sprague-Dawley, Maze Learning, Estrous Cycle, Rats

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Evaluation of estrous cycle stage and gender on behavioral outcome after experimental traumatic brain injury

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