Maternal Stress Combined with Terbutaline Leads to Comorbid Autistic-Like Behavior and Epilepsy in a Rat Model

被引:28
作者
Bercum, Florencia M. [1 ]
Rodgers, Krista M. [1 ]
Benison, Alex M. [1 ]
Smith, Zachariah Z. [1 ]
Taylor, Jeremy [1 ]
Kornreich, Elise [1 ]
Grabenstatter, Heidi L. [1 ]
Dudek, F. Edward [2 ]
Barth, Daniel S. [1 ]
机构
[1] Univ Colorado, Dept Psychol & Neurosci, Boulder, CO 80309 USA
[2] Univ Utah, Sch Med, Dept Neurosurg, Salt Lake City, UT 84108 USA
关键词
autism; epilepsy; maternal stress; neuroinflammation; terbutaline; PRENATAL STRESS; EPILEPTIFORM ACTIVITY; SPECTRUM DISORDERS; PREMATURE LABOR; CHILDREN; SEIZURES; BRAIN; RISK; NEUROINFLAMMATION; ABNORMALITIES;
D O I
10.1523/JNEUROSCI.2803-15.2015
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Human autism is comorbid with epilepsy, yet, little is known about the causes or risk factors leading to this combined neurological syndrome. Although genetic predisposition can play a substantial role, our objective was to investigate whether maternal environmental factors alone could be sufficient. We examined the independent and combined effects of maternal stress and terbutaline (used to arrest preterm labor), autism risk factors in humans, on measures of both autistic-like behavior and epilepsy in Sprague-Dawley rats. Pregnant dams were exposed to mild stress (foot shocks at 1 week intervals) throughout pregnancy. Pups were injected with terbutaline on postnatal days 2-5. Either maternal stress or terbutaline resulted in autistic-like behaviors in offspring (stereotyped/repetitive behaviors and deficits in social interaction or communication), but neither resulted in epilepsy. However, their combination resulted in severe behavioral symptoms, as well as spontaneous recurrent convulsive seizures in 45% and epileptiform spikes in 100%, of the rats. Hippocampal gliosis (GFAP reactivity) was correlated with both abnormal behavior and spontaneous seizures. We conclude that prenatal insults alone can cause comorbid autism and epilepsy but it requires a combination of teratogens to achieve this; testing single teratogens independently and not examining combinatorial effects may fail to reveal key risk factors in humans. Moreover, astrogliosis may be common to both teratogens. This new animal model of combined autism and epilepsy permits the experimental investigation of both the cellular mechanisms and potential intervention strategies for this debilitating comorbid syndrome.
引用
收藏
页码:15894 / 15902
页数:9
相关论文
共 54 条
[1]  
APA, 2013, DIAGN STAT MAN MENT
[2]   Stressed-out, or in (utero)? [J].
Avishai-Eliner, S ;
Brunson, KL ;
Sandman, CA ;
Baram, TZ .
TRENDS IN NEUROSCIENCES, 2002, 25 (10) :518-524
[3]   Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005-2009 [J].
Berg, Anne T. ;
Berkovic, Samuel F. ;
Brodie, Martin J. ;
Buchhalter, Jeffrey ;
Cross, J. Helen ;
Boas, Walter van Emde ;
Engel, Jerome ;
French, Jacqueline ;
Glauser, Tracy A. ;
Mathern, Gary W. ;
Moshe, Solomon L. ;
Nordli, Douglas ;
Plouin, Perrine ;
Scheffer, Ingrid E. .
EPILEPSIA, 2010, 51 (04) :676-685
[4]   Hippocampal pathology in refractory temporal lobe epilepsy - T2-weighted signal change reflects dentate gliosis [J].
Briellmann, RS ;
Kalnins, RM ;
Berkovic, SF ;
Jackson, GD .
NEUROLOGY, 2002, 58 (02) :265-271
[5]   Prenatal Stress-Induced Increases in Placental Inflammation and Offspring Hyperactivity Are Male-Specific and Ameliorated by Maternal Antiinflammatory Treatment [J].
Bronson, Stefanie L. ;
Bale, Tracy L. .
ENDOCRINOLOGY, 2014, 155 (07) :2635-2646
[6]   Communication of Adult Rats by Ultrasonic Vocalization: Biological, Sociobiological, and Neuroscience Approaches [J].
Brudzynski, Stefan M. .
ILAR JOURNAL, 2009, 50 (01) :43-50
[7]   Prenatal stress and brain development [J].
Charil, Arnaud ;
Laplante, David P. ;
Vaillancourt, Cathy ;
King, Suzanne .
BRAIN RESEARCH REVIEWS, 2010, 65 (01) :56-79
[8]   Safety Signals Mitigate the Consequences of Uncontrollable Stress Via a Circuit Involving the Sensory Insular Cortex and Bed Nucleus of the Stria Terminalis [J].
Christianson, John P. ;
Jennings, Joshua H. ;
Ragole, Thomas ;
Flyer, Johana G. N. ;
Benison, Alexander M. ;
Barth, Daniel S. ;
Watkins, Linda R. ;
Maier, Steven F. .
BIOLOGICAL PSYCHIATRY, 2011, 70 (05) :458-464
[9]   Translating developmental time across mammalian species [J].
Clancy, B ;
Darlington, RB ;
Finlay, BL .
NEUROSCIENCE, 2001, 105 (01) :7-17
[10]   The prevalence of autistic spectrum disorder in children surveyed in a tertiary care epilepsy clinic [J].
Clarke, DF ;
Roberts, W ;
Daraksan, M ;
Dupuis, A ;
McCabe, J ;
Wood, H ;
Snead, OC ;
Weiss, SK .
EPILEPSIA, 2005, 46 (12) :1970-1977