Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage
Abstract
Early brain damage, such as white matter damage (WMD), resulting from perinatal hypoxia-ischemia in preterm and low birth weight infants represents a high risk factor for mortality and chronic disabilities, including sensory, motor, behavioral and cognitive disorders. In previous studies, we developed a model of WMD based on prenatal ischemia (PI), induced by unilateral ligation of uterine artery at E17 in pregnant rats. We have shown that PI reproduced some of the main deficits observed in preterm infants, such as white and gray matter damage, myelination deficits, locomotor, sensorimotor, and short-term memory impairments, as well as related musculoskeletal and neuroanatomical histopathologies [1-3]. Here, we determined the deleterious impact of PI on several behavioral and cognitive abilities in adult rats, as well as on the neuroanatomical substratum in various related brain areas. Adult PI rats exhibited spontaneous exploratory and motor hyperactivity, deficits in information encoding, and deficits in short- and long-term object memory tasks, but no impairments in spatial learning or working memory in watermaze tasks. These results were in accordance with white matter injury and damage in the medial and lateral entorhinal cortices, as detected by axonal degeneration, astrogliosis and neuronal density. Although there was astrogliosis and axonal degeneration in the fornix, hippocampus and cingulate cortex, neuronal density in the hippocampus and cingulate cortex was not affected by PI. Levels of spontaneous hyperactivity, deficits in object memory tasks, neuronal density in the medial and lateral entorhinal cortices, and astrogliosis in the fornix correlated with birth weight in PI rats. Thus, this rodent model of WMD based on PI appears to recapitulate the main neurobehavioral and neuroanatomical human deficits often observed in preterm children with a perinatal history of ischemia.
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Multiple fetuses per pregnancy, intrauterine growth restriction (IUGR), X-ray, UV, nuclear or cosmic radiation, (ultra)sound as well as high temperature, preterm birth or hypoxia whether or not by traumatic causes can pose serious threats to proper corticogenesis.
“Multiple fetuses per pregnancy, intrauterine growth restriction (IUGR, due to placental failure other than by causes described above), X-ray, UV, nuclear or cosmic radiation, (ultra)sound as well as high temperature, preterm birth or hypoxia whether or not by traumatic causes can pose serious threats to proper corticogenesis as well [349–356].”
From Development of prefrontal cortex (2022) · cites this paper as [352]
Cites
Morris water maze: procedures for assessing spatial and related forms of learning and memory
Vorhees, C. V., & Williams, M. T. (2006) · Nature Protocols · doi:10.1038/nprot.2006.116 · Cited by 4,629 · see citing works
The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances
Volpe, J. J. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70294-1 · Cited by 2,420 · see citing works
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children
Aarnoudse-Moens, C. S. H., Weisglas-Kuperus, N., van Goudoever, J. B., & Oosterlaan, J. (2009) · Pediatrics · doi:10.1542/peds.2008-2816 · Cited by 1,587 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
Winters, B. D., Forwood, S., Cowell, R. A., Saksida, L. M., & Bussey, T. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1346-04.2004 · Cited by 588 · see citing works
Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
Winters, B. D., Saksida, L. M., & Bussey, T. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.004 · Cited by 574 · see citing works
The Parahippocampal Region: Corticocortical Connectivity
Burwell, R. D. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06717.x · Cited by 513 · see citing works
Winocur, G., Moscovitch, M., & Bontempi, B. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.016 · Cited by 486 · see citing works
The subplate and early cortical circuits
Kanold, P. O., & Luhmann, H. J. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153244 · Cited by 440 · see citing works
Perinatal Hypoxic-Ischemic Brain Damage: Evolution of an Animal Model
Vannucci, R. C., & Vannucci, S. J. (2005) · Developmental Neuroscience · doi:10.1159/000085978 · Cited by 424 · see citing works
Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome
Nosarti, C., Γιουρούκου, Έ., Healy, E., Rifkin, L., Walshe, M., Reichenberg, A., Chitnis, X. A., Williams, S., & Murray, R. M. (2007) · Brain · doi:10.1093/brain/awm282 · Cited by 414 · see citing works
Delobel‐Ayoub, M., Arnaud, C., White‐Koning, M., Casper, C., Pierrat, V., Garel, M., Burguet, A., Rozé, J., Matis, J., Picaud, J., et al. (2009) · PEDIATRICS · doi:10.1542/peds.2008-1216 · Cited by 399 · see citing works
Experimental growth retardation in the foetal rat
Wigglesworth, J. S. (1964) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700880102 · Cited by 372 · see citing works
Counsell, S. J., Edwards, A. D., Chew, A. T. M., Anjari, M., Dyet, L. E., Srinivasan, L., Boardman, J. P., Allsop, J. M., Hajnal, J. V., Rutherford, M., et al. (2008) · Brain · doi:10.1093/brain/awn268 · Cited by 279 · see citing works
Change in the Brain's White Matter
Fields, R. D. (2010) · Science · doi:10.1126/science.1199139 · Cited by 265 · see citing works
Towfighi, J., Mauger, D. T., Vannucci, R. C., & Vannucci, S. J. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00036-9 · Cited by 242 · see citing works
Impaired Spatial Learning and Hyperactivity in Developing Rats Exposed to Intermittent Hypoxia
Row, B. W., Kheirandish, L., Neville, J. J., & Gozal, D. (2002) · Pediatric Research · doi:10.1203/00006450-200209000-00024 · Cited by 239 · see citing works
Schmajuk, N. A. (1998) · Cited by 225 · see citing works
Derrick, M., Luo, N. L., Bregman, J. C., Jilling, T., Ji, X., Fisher, K., Gladson, C. L., Beardsley, D. J., MURDOCH, G. H., Back, S. A., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2816-03.2004 · Cited by 221 · see citing works
A Neural Circuit Basis for Spatial Working Memory
Constantinidis, C., & Wang, X. (2004) · The Neuroscientist · doi:10.1177/1073858404268742 · Cited by 212 · see citing works
Cognitive visual dysfunctions in preterm children with periventricular leukomalacia
Fazzi, E. M., Bova, S. M., Giovenzana, A., et al. (2009) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2009.03272.x · Cited by 193 · see citing works
Emerging concepts in periventricular white matter injury
Back, S. A., & Rivkees, S. A. (2004) · Seminars in Perinatology · doi:10.1053/j.semperi.2004.10.010 · Cited by 192 · see citing works
Overview of Animal Models of Attention Deficit Hyperactivity Disorder (ADHD)
Russell, V. A. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0935s54 · Cited by 176 · see citing works
Warburton, E. C., & Brown, M. W. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.12.022 · Cited by 166 · see citing works
Perinatal Subplate Neuron Injury: Implications for Cortical Development and Plasticity
McQuillen, P. S., & Ferriero, D. M. (2005) · Brain Pathology · doi:10.1111/j.1750-3639.2005.tb00528.x · Cited by 155 · see citing works
Woodward, L. J., Clark, C. A. C., Pritchard, V. E., Anderson, P. J., & Inder, T. E. (2011) · Developmental Neuropsychology · doi:10.1080/87565641.2011.540530 · Cited by 153 · see citing works
Long-lasting behavioral alterations following a hypoxic/ischemic brain injury in neonatal rats
Balduini, W., Angelis, V. D., Mazzoni, E., & Cimino, M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)01997-1 · Cited by 144 · see citing works
Decreased Regional Brain Volume and Cognitive Impairment in Preterm Children at Low Risk
Soria‐Pastor, S., Padilla, N., Zubiaurre‐Elorza, L., Ibarretxe‐Bilbao, N., Botet, F., Moragas, C. C. I., Falcón, C., Bargalló, N., Mercader, J. M., & Junqué, C. (2009) · PEDIATRICS · doi:10.1542/peds.2009-0244 · Cited by 136 · see citing works
Dell'Anna, M. E., Calzolari, S., Molinari, M., Iuvone, L., & Calimici, R. (1991) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80078-6 · Cited by 133 · see citing works
Brake, W. G., Sullivan, R. M., & Gratton, A. P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-14-05538.2000 · Cited by 131 · see citing works
Pereira, L. O., Arteni, N. S., Petersen, R. C., da Rocha, A. P., Achaval, M., & Netto, C. A. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.07.003 · Cited by 129 · see citing works
Hunsaker, M. R., Mooy, G. G., Swift, J. S., & Kesner, R. P. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.4.742 · Cited by 128 · see citing works
Sullivan, R. M., & Brake, W. G. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.015 · Cited by 126 · see citing works
The Medial Prefrontal Cortex Is Involved in Spatial Memory Retrieval under Partial-Cue Conditions
Jo, Y. S., Park, E., Kim, I. H., Park, S. K., Kim, H., Kim, H. T., & Choi, J.-S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3589-07.2007 · Cited by 123 · see citing works
Hypoxia-ischemia induced neurological dysfunction and brain injury in the neonatal rat
FAN, L., Lin, S., Pang, Y., et al. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.033 · Cited by 122 · see citing works
A comparison of executive function in very preterm and term infants at 8 months corrected age
Sun, J., Mohay, H. A., & O'Callaghan, M. J. (2008) · Early Human Development · doi:10.1016/j.earlhumdev.2008.10.005 · Cited by 119 · see citing works
Beaino, G., Khoshnood, B., Kaminski, M., Marret, S., Pierrat, V., Vieux, R., Thiriez, G., Matis, J., Picaud, J., Rozé, J., et al. (2011) · Acta Paediatrica · doi:10.1111/j.1651-2227.2010.02064.x · Cited by 116 · see citing works
Golan, H. M., & Huleihel, M. (2006) · Developmental Science · doi:10.1111/j.1467-7687.2006.00498.x · Cited by 112 · see citing works
Shultz, S. R., MacFabe, D. F., Foley, K. A., Taylor, R., & Cain, D. P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.06.012 · Cited by 112 · see citing works
Hippocampal damage and anterograde object-recognition in rats after long retention intervals
Mumby, D. G., Tremblay, A., Lecluse, V., & Lehmann, H. (2005) · Hippocampus · doi:10.1002/hipo.20122 · Cited by 112 · see citing works
The role of rat dorsomedial prefrontal cortex in spatial working memory
Horst, N. K., & Laubach, M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.004 · Cited by 109 · see citing works
Prenatal Ischemia and White Matter Damage in Rats
Olivier, P., Baud, O., Evrard, P., Gressèns, P., & Verney, C. (2005) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000187052.81889.57 · Cited by 104 · see citing works
Self-citationWeible, A. P., Rowland, D. C., Pang, R. D., & Kentros, C. G. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00214.2009 · Cited by 99 · see citing works
Panksepp, J., Burgdorf, J. S., Turner, C. A., & Gordon, N. S. (2003) · Brain and Cognition · doi:10.1016/s0278-2626(03)00013-7 · Cited by 92 · see citing works
White Matter Injury Correlates with Hypertonia in an Animal Model of Cerebral Palsy
Drobyshevsky, A., Derrick, M., Wyrwicz, A. M., Ji, X., Englöf, I., Ullman, L. M., Zelaya, M. E., Northington, F. J., & Tan, S. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600333 · Cited by 90 · see citing works
Molecular Mechanisms Involved in Injury to the Preterm Brain
Kaindl, A. M., Favrais, G., & Gressèns, P. (2009) · Journal of Child Neurology · doi:10.1177/0883073809337920 · Cited by 86 · see citing works
Developmental changes induced by graded prenatal systemic hypoxic–ischemic insults in rats
Robinson, S., Rubin, K. P., Li, Q., Cohen, M. L., DeChant, A. K., Tabrizi, N., Bucek, M., Lust, D. W., & Miller, R. H. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.10.024 · Cited by 85 · see citing works
Diffusion tensor MRI of the corpus callosum and cognitive function in adults born preterm
Kontis, D., Catani, M., Cuddy, M., et al. (2009) · Neuroreport · doi:10.1097/wnr.0b013e328325a8f9 · Cited by 85 · see citing works
Pires, V. A., Pamplona, F. A., Pandolfo, P., Fernandes, D., Prediger, R. D., & Takahashi, R. N. (2009) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32832a80bf · Cited by 84 · see citing works
Parron, C., & Save, É. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.004 · Cited by 76 · see citing works
Bardgett, M. E., Davis, N. N., Schultheis, P. J., & Griffith, M. S. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.10.008 · Cited by 67 · see citing works
Cai, Z., Xiao, F., Lee, B., et al. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00076-3 · Cited by 64 · see citing works
Delcour, M., Olivier, P., Chambon, C., Pansiot, J., Russier, M., Liberge, M., Xin, D., Gestreau, C., Alescio‐Lautier, B., Gressèns, P., et al. (2011) · Brain Pathology · doi:10.1111/j.1750-3639.2011.00504.x · Cited by 62 · see citing works
Self-citationMorales, P., Fiedler, J. L., Andrés, S., et al. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21715 · Cited by 57 · see citing works
Chang, Y., Tzeng, S., Yu, L., Huang, A., Lee, H., Huang, C., & Ho, C.-J. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.06.001 · Cited by 54 · see citing works
Pavlova, M. A., Sokolov, A. N., & Krägeloh‐Mann, I. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj153 · Cited by 49 · see citing works
Acute perinatal asphyxia impairs non-spatial memory and alters motor coordination in adult male rats
Simola, N., Bustamante, D., Pinna, A., Pontis, S., Morales, P., Morelli, M., & Herrera‐Marschitz, M. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-1186-7 · Cited by 48 · see citing works
Neuroprotective Effect of Inhaled Nitric Oxide on Excitotoxic-Induced Brain Damage in Neonatal Rat
Pansiot, J., Loron, G., Olivier, P., Fontaine, R. H., Charriaut‐Marlangue, C., Mercier, J., Gressèns, P., & Baud, O. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010916 · Cited by 46 · see citing works
Self-citationOn familiarity and recall of events by rats
Eacott, M. J., & Easton, A. (2007) · Hippocampus · doi:10.1002/hipo.20325 · Cited by 42 · see citing works
Robinson, S. (2005) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2005.06.005 · Cited by 33 · see citing works
The structure of memory in infants and toddlers: an SEM study with full-terms and preterms
Rose, S. A., Feldman, J. F., Jankowski, J. J., & Rossem, R. V. (2010) · Developmental Science · doi:10.1111/j.1467-7687.2010.00959.x · Cited by 32 · see citing works
Elliott, M. B., Jallo, J., Barbe, M. F., & Tuma, R. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.104 · Cited by 29 · see citing works
Self-citationDelcour, M., Russier, M., Xin, D., et al. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.02.010 · Cited by 29 · see citing works
Self-citationBehavioral Effects of Basal Forebrain Cholinergic Lesions in Young Adult and Aging Rats.
Paban, V., Chambon, C., Jaffard, M., et al. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.933 · Cited by 27 · see citing works
Self-citationHutton, L. C., Ratnayake, U., Shields, A., et al. (2009) · Developmental Neuroscience · doi:10.1159/000251907 · Cited by 18 · see citing works
Arco, A. D., Ronzoni, G., & Mora, F. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2055-9 · Cited by 18 · see citing works
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- Authors
- Delcour, M., Russier, M., Amin, M., Baud, O., Paban, V., Barbe, M. F., & Coq, J.-O.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Temple University (US)
- Inserm (FR)
- Corresponding author
- Coq, Jacques-Olivier
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 232
- Issue
- 1
- Pages
- 233-244
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2051713219
- Cited by
- 72
- References
- 68
- Citations by year
- 2026: 1 · 2024: 8 · 2023: 6 · 2022: 5 · 2021: 8 · 2020: 4 · 2019: 1 · 2018: 8 · 2017: 10 · 2016: 6 · 2015: 6 · 2014: 3 · 2013: 4 · 2012: 2
- FWCI
- 4.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Aix-Marseille Université
- Temple University
- Ministère de l'Enseignement Supérieur et de la Recherche
- Centre National de la Recherche Scientifique
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Development and Preterm Care
- Keywords
- white matter injury, perinatal hypoxia-ischemia, preterm infants, low birth weight, entorhinal cortex, astrocyte activation, axonal degeneration, fornix, hippocampus, cingulate cortex, neurobehavioral deficits, rodent models
- MeSH terms
- Animals, Behavior, Animal, Brain, Brain Damage, Chronic, Brain Ischemia, Cognition, Cues, Female, Fluoresceins, Gliosis, Immunohistochemistry, Memory, Motor Activity, Organic Chemicals, Pregnancy, Prenatal Exposure Delayed Effects, Reversal Learning, Space Perception, Rats, Sprague-Dawley, Maze Learning, Recognition, Psychology, Rats, Memory, Long-Term
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