Hyperactivation of the amygdala correlates with impaired social play behavior of prepubertal male rats in a maternal immune activation model

Blanc, 2005, Dysregulation of pretend play and communication development in children with autism, Autism, 9, 229, 10.1177/1362361305053253 Loomes, 2017, What is the male-to-Female ratio in autism Spectrum disorder? A systematic review and meta-analysis, J. Am. Acad. Child Adolesc. Psychiatry, 56, 466, 10.1016/j.jaac.2017.03.013 Bjørklund, 2018, Diagnostic and severity-tracking biomarkers for autism Spectrum disorder, J. Mol. Neurosci., 66, 492, 10.1007/s12031-018-1192-1 Persico, 2006, Searching for ways out of the autism maze: genetic, epigenetic and environmental clues, Trends Neurosci., 29, 349, 10.1016/j.tins.2006.05.010 Dufour-Rainfray, 2011, Foetal exposure to teratogens: evidence of genes involved in autism, Neurosci. Biobehav. Rev., 35, 1254, 10.1016/j.neubiorev.2010.12.013 Jiang, 2016, Maternal infection during pregnancy and risk of autism spectrum disorders: a systematic review and meta-analysis, Brain Behav. Immun., 58, 165, 10.1016/j.bbi.2016.06.005 Miller, 2017, The immunology of behavior-exploring the role of the immune system in brain health and illness, Neuropsychopharmacology, 42, 1, 10.1038/npp.2016.229 Cieślik, 2020, Maternal immune activation induces neuroinflammation and cortical synaptic deficits in the adolescent rat offspring, Int. J. Mol. Sci., 21, 4097, 10.3390/ijms21114097 Bateson, 2015, Playfulness and creativity, Curr. Biol., 25, R12, 10.1016/j.cub.2014.09.009 Burghardt, 2010, The comparative reach of play and brain: perspective, evidence and implications, Am. J. Play, 2, 338 Pellis, 1998, Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses, Neurosci. Biobehav. Rev., 23, 87, 10.1016/S0149-7634(97)00071-7 Vanderschuren, 2014, What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms, Curr. Top. Behav. Neurosci., 16, 189, 10.1007/978-3-662-45758-0_268 Trezza, 2010, The pleasures of play: pharmacological insights into social reward mechanisms, Trends Pharmacol. Sci., 31, 463, 10.1016/j.tips.2010.06.008 Kirsten, 2017, Prenatal lipopolysaccharide induces hypothalamic dopaminergic hypoactivity and autistic-like behaviors: repetitive self-grooming and stereotypies, Behav. Brain Res., 331, 25, 10.1016/j.bbr.2017.05.013 Gumusoglu, 2019, Maternal inflammation and neurodevelopmental programming: a review of preclinical outcomes and implications for translational psychiatry, Biol. Psychiatry, 85, 107, 10.1016/j.biopsych.2018.08.008 Blake, 2015, Hormonal programming of rat social play behavior: standardized techniques will aid synthesis and translation to human health, Neurosci. Biobehav. Rev., 55, 184, 10.1016/j.neubiorev.2015.04.021 Libby, 1998, Spontaneous play in children with autism: a reappraisal, J. Autism Dev. Disord., 28, 487, 10.1023/A:1026095910558 Williams, 2003, A comparative review of early forms of object-directed play and parent-infant play in typical infants and young children with autism, Autism, 7, 361, 10.1177/1362361303007004003 Jordan, 2003, Social play and autistic spectrum disorders: a perspective on theory, implications and educational approaches, Autism, 7, 347, 10.1177/1362361303007004002 Stahmer, 2003, Behavioral approaches to promoting play, Autism, 7, 401, 10.1177/1362361303007004006 MacDonald, 2017, Child behaviors of young children with autism spectrum disorder across play Settings, Adapt. Phys. Activ. Q., 34, 19 Memari, 2015, Children with autism spectrum disorder and patterns of participation in daily physical and play activities, Neurol. Res. Int., 2015, 10.1155/2015/531906 Servadio, 2015, Modeling autism-relevant behavioral phenotypes in rats and mice: Do’ autistic’ rodents exist?, Behav. Pharmacol., 26, 522, 10.1097/FBP.0000000000000163 Melancia, 2018, Sex-specific autistic endophenotypes induced by prenatal exposure to valproic acid involve anandamide signalling, Br. J. Pharmacol., 175, 3699, 10.1111/bph.14435 Schiavi, 2019, Reward-related behavioral, neurochemical and electrophysiological changes in a rat model of autism based on prenatal exposure to valproic acid, Front. Cell. Neurosci., 13, 479, 10.3389/fncel.2019.00479 Gzielo, 2020, Valproic acid exposure impairs ultrasonic communication in infant, adolescent and adult rats, Eur. Neuropsychopharmacol., 41, 52, 10.1016/j.euroneuro.2020.09.006 Pletnikov, 1999, Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: a model of autism, Behav. Brain Res., 100, 43, 10.1016/S0166-4328(98)00111-9 Kirsten, 2012, Hypoactivity of the central dopaminergic system and autistic-like behavior induced by a single early prenatal exposure to lipopolysaccharide, J. Neurosci. Res., 90, 1903, 10.1002/jnr.23089 van Tilborg, 2018, Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism-like behavior in a rat model of diffuse white matter injury, Glia, 66, 78, 10.1002/glia.23216 Breach, 2021, Maternal allergic inflammation in rats impacts the offspring perinatal neuroimmune milieu and the development of social play, locomotor behavior, and cognitive flexibility, Brain Behav. Immun., 95, 269, 10.1016/j.bbi.2021.03.025 Gzielo, 2021, The effect of maternal immune activation on social play-induced ultrasonic vocalization in rats, Brain Sci., 11, 344, 10.3390/brainsci11030344 Beloosesky, 2010, Maternal lipopolysaccharide-induced inflammation during pregnancy programs impaired offspring innate immune responses, Am. J. Obstet. Gynecol., 203 Baharnoori, 2012, Neonatal behavioral changes in rats with gestational exposure to lipopolysaccharide: a prenatal infection model for developmental neuropsychiatric disorders, Schizophr. Bull., 38, 444, 10.1093/schbul/sbq098 Kentner, 2019, Maternal immune activation: reporting guidelines to improve the rigor, reproducibility, and transparency of the model, Neuropsychopharmacology, 44, 245, 10.1038/s41386-018-0185-7 de Ávila, 2020, Prenatal exposure to alcohol impairs social play behavior in adolescent male mice, Neurotoxicology, 79, 142, 10.1016/j.neuro.2020.05.007 Costa, 2013, Continuous central infusion of cannabinoid receptor agonist WIN 55,212-2 decreases maternal care in lactating rats: consequences for fear conditioning in adulthood males, Behav. Brain Res., 257, 31, 10.1016/j.bbr.2013.09.022 Batista, 2019, Maternal protein malnutrition induces autism-like symptoms in rat offspring, Nutr. Neurosci., 22, 655, 10.1080/1028415X.2018.1427660 Melancia, 2017, Testing the correlation between experimentally-induced hypothyroidism during pregnancy and autistic-like symptoms in the rat offspring, Behav. Brain Res., 321, 113, 10.1016/j.bbr.2016.12.032 Walf, 2007, The use of the elevated plus maze as an assay of anxiety-related behavior in rodents, Nat. Protoc., 2, 322, 10.1038/nprot.2007.44 Ribeiro, 2020, Metabolic syndrome accentuates post-traumatic stress disorder-like symptoms and glial activation, Behav. Brain Res., 384 Carvalho, 2016, Early life overnutrition induced by litter size manipulation decreases social play behavior in adolescent male rats, Int. J. Dev. Neurosci., 53, 75, 10.1016/j.ijdevneu.2016.07.005 van Kerkhof, 2013, Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum, Neuropsychopharmacology, 38, 1899, 10.1038/npp.2013.83 Vanderschuren, 1995, Sequential analysis of social play behavior in juvenile rats: effects of morphine, Behav. Brain Res., 72, 89, 10.1016/0166-4328(96)00060-5 Vilela, 2014, Cannabinoid receptor agonist disrupts behavioral and neuroendocrine responses during lactation, Behav. Brain Res., 263, 190, 10.1016/j.bbr.2014.01.037 Paxinos, 1997 Hopkins, 2009, Progressive statistics for studies in sports medicine and exercise science, Med. Sci. Sports Exerc., 41, 3, 10.1249/MSS.0b013e31818cb278 Oishi, 2013, Role of the medial prefrontal cortex in cataplexy, J. Neurosci., 33, 9743, 10.1523/JNEUROSCI.0499-13.2013 Smith, 2007, Maternal immune activation alters fetal brain development through interleukin-6, J. Neurosci., 27, 10695, 10.1523/JNEUROSCI.2178-07.2007 Machado, 2015, Maternal immune activation in nonhuman primates alters social attention in juvenile offspring, Biol. Psychiatry, 77, 823, 10.1016/j.biopsych.2014.07.035 Careaga, 2018, Variability in PolyIC induced immune response: implications for preclinical maternal immune activation models, J. Neuroimmunol., 15, 87, 10.1016/j.jneuroim.2018.06.014 Keever, 2020, Lasting and sex-dependent impact of maternal immune activation on molecular pathways of the Amygdala, Front. Neurosci., 14, 774, 10.3389/fnins.2020.00774 Thom, 2020, Immune modulatory treatments for autism Spectrum disorder, Semin. Pediatr. Neurol., 35, 10.1016/j.spen.2020.100836 Garami, 2018, Fever and hypothermia in systemic inflammation, Handb. Clin. Neurol., 157, 565, 10.1016/B978-0-444-64074-1.00034-3 Oliveira, 2020, Simvastatin attenuated sickness behavior and fever in a murine model of endotoxemia, Life Sci., 254, 10.1016/j.lfs.2020.117701 Silver, 1994, Lipopolysaccharide-induced fetal death: the role of tumor-necrosis factor alpha, Biol. Reprod., 50, 1108, 10.1095/biolreprod50.5.1108 Xu, 2007, Effects of low-dose lipopolysaccharide (LPS) pretreatment on LPS-induced intra-uterine fetal death and preterm labor, Toxicology, 234, 167, 10.1016/j.tox.2007.02.010 Carpentier, 2011, Placental TNF-α signaling in illness-induced complications of pregnancy, Am. J. Pathol., 178, 2802, 10.1016/j.ajpath.2011.02.042 French, 2013, Maternal immune activation affects litter success, size and neuroendocrine responses related to behavior in adult offspring, Physiol. Behav., 119, 175, 10.1016/j.physbeh.2013.06.018 Kirsten, 2015, Prenatal zinc prevents communication impairments and BDNF disturbance in a rat model of autism induced by prenatal lipopolysaccharide exposure, Life Sci., 130, 12, 10.1016/j.lfs.2015.02.027 Lins, 2018, Prospective analysis of the effects of maternal immune activation on rat cytokines during pregnancy and behavior of the male offspring relevant to schizophrenia, eNeuro, 5, 10.1523/ENEURO.0249-18.2018 Keller, 2019, The parental brain and behavior: a target for endocrine disruption, Front. Neuroendocrinol., 54, 10.1016/j.yfrne.2019.100765 Smith, 2004, Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats, Psychoneuroendocrinology, 29, 227, 10.1016/S0306-4530(03)00025-8 Brouette-Lahlou, 1999, The mother rat’s vomeronasal organ is involved in detection of dodecyl propionate, the pup’s preputial gland pheromone, Physiol. Behav., 66, 427, 10.1016/S0031-9384(98)00334-5 Moore, 1979, Mother rats interact differently with male and female offspring, J. Comp. Physiol. Psychol., 93, 677, 10.1037/h0077599 Smotherman, 1974, Maternal responses to infant vocalizations and olfactory cues in rats and mice, Behav. Biol., 12, 55, 10.1016/S0091-6773(74)91026-8 Ehret, 2005, Infant rodent ultrasounds -- a gate to the understanding of sound communication, Behav. Genet., 35, 19, 10.1007/s10519-004-0853-8 Champagne, 2003, Variations in maternal care in the rat as a mediating influence for the effects of environment on development, Physiol. Behav., 79, 359, 10.1016/S0031-9384(03)00149-5 Liu, 2000, Maternal care, hippocampal synaptogenesis and cognitive development in rats, Nat. Neurosci., 3, 799, 10.1038/77702 Champagne, 2008, Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress, J. Neurosci., 28, 6037, 10.1523/JNEUROSCI.0526-08.2008 Caldji, 1998, Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat, Proc. Natl. Acad. Sci. U. S. A., 95, 5335, 10.1073/pnas.95.9.5335 Weaver, 2006, Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood, Proc. Natl. Acad. Sci. U. S. A., 103, 3480, 10.1073/pnas.0507526103 van Hasselt, 2011, Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats, Physiol. Behav., 106, 701, 10.1016/j.physbeh.2011.12.007 Sequeira-Cordero, 2013, Maternal behavior as an early modulator of neurobehavioral offspring responses by Sprague-Dawley rats, Behav. Brain Res., 237, 63, 10.1016/j.bbr.2012.09.028 Nguyen, 2015, Maternal care differentially affects neuronal excitability and synaptic plasticity in the dorsal and ventral hippocampus, Neuropsychopharmacology, 40, 1590, 10.1038/npp.2015.19 Premoli, 2019, Specific profile of ultrasonic communication in a mouse model of neurodevelopmental disorders, Sci. Rep., 9, 15912, 10.1038/s41598-019-52378-0 Kirsten, 2011, Prenatal LPS exposure reduces olfactory perception in neonatal and adult rats, Physiol. Behav., 104, 417, 10.1016/j.physbeh.2011.04.049 Carlezon, 2019, Maternal and early postnatal immune activation produce sex-specific effects on autism-like behaviors and neuroimmune function in mice, Sci. Rep., 9, 16928, 10.1038/s41598-019-53294-z Hartley, 2009, Sex differences in autism spectrum disorder: an examination of developmental functioning, autistic symptoms, and coexisting behavior problems in toddlers, J. Autism Dev. Disord., 39, 1715, 10.1007/s10803-009-0810-8 Supekar, 2015, Sex differences in structural organization of motor systems and their dissociable links with repetitive/restricted behaviors in children with autism, Mol. Autism, 6, 50, 10.1186/s13229-015-0042-z South, 2011, Failure is not an option: risk-taking is moderated by anxiety and also by cognitive ability in children and adolescents diagnosed with an autism spectrum disorder, J. Autism Dev. Disord., 41, 55, 10.1007/s10803-010-1021-z Lai, 2014, Autism, Lancet, 383, 896, 10.1016/S0140-6736(13)61539-1 Guan, 2017, Injury mortality in individuals with autism, Am. J. Public Health, 107, 791, 10.2105/AJPH.2017.303696 Oron, 2019, Gene network analysis reveals a role for striatal glutamatergic receptors in dysregulated risk-assessment behavior of autism mouse models, Transl. Psychiatry, 9, 257, 10.1038/s41398-019-0584-5 Panksepp, 1984, The psychobiology of play: theoretical and methodological perspectives, Neurosci. Biobehav. Rev., 8, 465, 10.1016/0149-7634(84)90005-8 Vanderschuren, 1997, The neurobiology of social play behavior in rats, Neurosci. Biobehav. Rev., 21, 309, 10.1016/S0149-7634(96)00020-6 Bell, 2009, The role of the medial prefrontal cortex in the play fighting of rats, Behav. Neurosci., 123, 1158, 10.1037/a0017617 van Kerkhof, 2014, Cellular activation in limbic brain systems during social play behaviour in rats, Brain Struct. Funct., 219, 1181 Pellis, 1993, The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats, Neurosci. Lett., 158, 13, 10.1016/0304-3940(93)90600-P van Kerkhof, 2013, Functional integrity of the habenula is necessary for social play behaviour in rats, Eur. J. Neurosci., 38, 3465, 10.1111/ejn.12353 Achterberg, 2018, On the central noradrenergic mechanism underlying the social play-suppressant effect of methylphenidate in rats, Behav. Brain Res., 347, 158, 10.1016/j.bbr.2018.03.004 Felix-Ortiz, 2016, Bidirectional modulation of anxiety-related and social behaviors by amygdala projections to the medial prefrontal cortex, Neuroscience, 321, 197, 10.1016/j.neuroscience.2015.07.041 Hoover, 2007, Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat, Brain Struct. Funct., 212, 149, 10.1007/s00429-007-0150-4 Gehrlach, 2020, A whole-brain connectivity map of mouse insular cortex, Elife, 9, 10.7554/eLife.55585 Baron-Cohen, 2000, The amygdala theory of autism, Neurosci. Biobehav. Rev., 24, 355, 10.1016/S0149-7634(00)00011-7 Schumann, 2004, The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages, J. Neurosci., 24, 6392, 10.1523/JNEUROSCI.1297-04.2004 Richter, 2015, Reduced cortical thickness and its association with social reactivity in children with autism spectrum disorder, Psychiatry Res., 234, 15, 10.1016/j.pscychresns.2015.06.011 Sharp, 2017, Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction, Transl. Psychiatry, 7, e1194, 10.1038/tp.2017.161 Ibrahim, 2019, Reduced amygdala-prefrontal functional connectivity in children with autism Spectrum disorder and Co-occurring disruptive behavior, Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 4, 1031 Bartolotti, 2020, Functional brain abnormalities associated with comorbid anxiety in autism spectrum disorder, Dev. Psychopathol., 32, 1273, 10.1017/S0954579420000772 Gordon, 2002, Expression of c-fos gene activation during rough and tumble play in juvenile rats, Brain Res. Bull., 57, 651, 10.1016/S0361-9230(01)00762-6 Huang, 2016, Hyperconnectivity of prefrontal cortex to amygdala projections in a mouse model of macrocephaly/autism syndrome, Nat. Commun., 7, 13421, 10.1038/ncomms13421 Lin, 2013, The amygdala excitatory/inhibitory balance in a valproate-induced rat autism model, PLoS One, 8 Meaney, 1981, Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats, Physiol. Behav., 26, 467, 10.1016/0031-9384(81)90175-X Paine, 2017, Decreasing GABA function within the medial prefrontal cortex or basolateral amygdala decreases sociability, Behav. Brain Res., 317, 542, 10.1016/j.bbr.2016.10.012