Effects of Cacna1c haploinsufficiency on social interaction behavior and 50-kHz ultrasonic vocalizations in adult female rats

Eaton, 2012, An invariant dimensional liability model of gender differences in mental disorder prevalence: evidence from a national sample, J. Abnorm. Psychol., 121, 282, 10.1037/a0024780 Steel, 2014, The global prevalence of common mental disorders: a systematic review and meta-analysis 1980–2013, Int. J. Epidemiol., 43, 476, 10.1093/ije/dyu038 Halladay, 2015, Sex and gender differences in autism spectrum disorder: summarizing evidence gaps and identifying emerging areas of priority, Mol. Autism, 6, 36, 10.1186/s13229-015-0019-y Abel, 2010, Sex differences in schizophrenia, Int. J. Soc. Psychiatry, 22, 417 Kennedy, 2012, The social brain in psychiatric and neurological disorders, Trends Cogn. Sci., 16, 559, 10.1016/j.tics.2012.09.006 Meyer-Lindenberg, 2012, Neural mechanisms of social risk for psychiatric disorders, Nat. Neurosci., 15, 663, 10.1038/nn.3083 Cross-Disorder Group of the Psychiatric Genomics Consortium, 2013, Identification of risk loci with shared effects on five major psychiatric disorders: a genome-wide analysis, Lancet, 381, 1371, 10.1016/S0140-6736(12)62129-1 Gandal, 2018, Shared molecular neuropathology across major psychiatric disorders parallels polygenic overlap, Science, 359, 693, 10.1126/science.aad6469 Ferreira, 2008, Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder, Nat. Genet., 40, 1056, 10.1038/ng.209 Splawski, 2004, Cav1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism, Cell, 119, 19, 10.1016/j.cell.2004.09.011 Nyegaard, 2010, CACNA1C (rs1006737) is associated with schizophrenia, Mol. Psychiatry, 15, 119, 10.1038/mp.2009.69 Green, 2010, The bipolar disorder risk allele at CACNA1C also confers risk of recurrent major depression and of schizophrenia, Mol. Psychiatry, 15, 1016, 10.1038/mp.2009.49 Dao, 2010, Mood disorder susceptibility gene CACNA1C modifies mood-related behaviors in mice and interacts with sex to influence behavior in mice and diagnosis in humans, Biol. Psychiatry, 68, 801, 10.1016/j.biopsych.2010.06.019 Witt, 2014, Analysis of genome-wide significant bipolar disorder genes in borderline personality disorder, Psychiatr. Genet., 24, 262, 10.1097/YPG.0000000000000060 Heilbronner, 2015, A common risk variant in CACNA1C supports a sex-dependent effect on longitudinal functioning and functional recovery from episodes of schizophrenia-spectrum but not bipolar disorder, Eur. Neuropsychopharmacol., 25, 2262, 10.1016/j.euroneuro.2015.09.012 Takeuchi, 2018, A common CACNA1C gene risk variant has sex-dependent effects on behavioral traits and brain functional activity, Cereb. Cortex, 1 Heyes, 2015, Genetic disruption of voltage-gated calcium channels in psychiatric and neurological disorders, Prog. Neurobiol., 134, 36, 10.1016/j.pneurobio.2015.09.002 Kabir, 2017, From gene to behavior: L-type calcium channel mechanisms underlying neuropsychiatric symptoms, Neurotherapeutics, 14, 588, 10.1007/s13311-017-0532-0 Kabir, 2016, L-type Ca 2+ channels in mood, cognition and addiction: integrating human and rodent studies with a focus on behavioural endophenotypes, J. Physiol., 594, 5823, 10.1113/JP270673 Pasparakis, 2015, The effects of the CACNA1C rs1006737 A/G on affective startle modulation in healthy males, Eur. Psychiatry, 30, 492, 10.1016/j.eurpsy.2015.03.004 Krug, 2010, Effect of CACNA1C rs1006737 on neural correlates of verbal fluency in healthy individuals, Neuroimage, 49, 1831, 10.1016/j.neuroimage.2009.09.028 Krautheim, 2018, Outgroup emotion processing in the vACC is modulated by childhood trauma and CACNA1C risk variant, Soc. Cogn. Affect. Neurosci., 13, 341, 10.1093/scan/nsy004 Bader, 2011, Mouse model of Timothy syndrome recapitulates triad of autistic traits, Proc. Natl. Acad. Sci., 108, 15432, 10.1073/pnas.1112667108 Kabitzke, 2018, Comprehensive analysis of two Shank3 and the Cacna1c mouse models of autism spectrum disorder, Genes Brain Behav., 17, 4, 10.1111/gbb.12405 Dedic, 2018, Cross-disorder risk gene CACNA1C differentially modulates susceptibility to psychiatric disorders during development and adulthood, Mol. Psychiatry, 23, 533, 10.1038/mp.2017.133 Jeon, 2010, Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC, Nat. Neurosci., 13, 482, 10.1038/nn.2504 Terrillion, 2017, Decreased nucleus accumbens expression of psychiatric disorder risk gene Cacna1c promotes susceptibility to social stress, Int. J. Neuropsychopharmacol., 20, 428, 10.1093/ijnp/pyw112 Kabir, 2017, Rescue of impaired sociability and anxiety-like behavior in adult cacna1c-deficient mice by pharmacologically targeting eIF2α, Mol. Psychiatry, 22, 1096, 10.1038/mp.2017.124 Moon, 2018, CACNA1C: Association With Psychiatric Disorders, Behavior, and Neurogenesis, Schizophr. Bull., 44, 958, 10.1093/schbul/sby096 McCullough, 2014, NIH initiative to balance sex of animals in preclinical studies: generative questions to guide policy, implementation, and metrics, Biol. Sex Differ., 5, 15, 10.1186/s13293-014-0015-5 Ellenbroek, 2016, Rodent models in neuroscience research: is it a rat race?, Dis. Model. Mech., 9, 1079, 10.1242/dmm.026120 Wöhr, 2013, Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation, Cell Tissue Res., 354, 81, 10.1007/s00441-013-1607-9 Kroes, 2007, Social defeat, a paradigm of depression in rats that elicits 22-kHz vocalizations, preferentially activates the cholinergic signaling pathway in the periaqueductal gray, Behav. Brain Res., 182, 290, 10.1016/j.bbr.2007.03.022 Blanchard, 1991, Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems, Physiol. Behav., 50, 967, 10.1016/0031-9384(91)90423-L Wöhr, 2008, Ultrasonic calling during fear conditioning in the rat: no evidence for an audience effect, Anim. Behav., 76, 749, 10.1016/j.anbehav.2008.04.017 Brudzynski, 2013, Ethotransmission: communication of emotional states through ultrasonic vocalization in rats, Curr. Opin. Neurobiol., 23, 310, 10.1016/j.conb.2013.01.014 Panksepp, 2005, Affective consciousness: core emotional feelings in animals and humans, Conscious. Cogn., 14, 30, 10.1016/j.concog.2004.10.004 Lukas, 2015, Endogenous vasopressin, innate anxiety, and the emission of pro-social 50-kHz ultrasonic vocalizations during social play behavior in juvenile rats, Psychoneuroendocrinology, 56, 35, 10.1016/j.psyneuen.2015.03.005 Knutson, 1998, Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats, J. Comp. Psychol., 112, 65, 10.1037/0735-7036.112.1.65 Thomas, 1985, Ultrasonic vocalization of the female rat (Rattus norvegicus) during mating, Anim. Behav., 33, 720, 10.1016/S0003-3472(85)80002-6 White, 1990, Changes in mating vocalizations over the ejaculatory series in rats (Rattus norvegicus), J. Comp. Psychol., 104, 255, 10.1037/0735-7036.104.3.255 Engelhardt, 2017, Effects of amphetamine on pro-social ultrasonic communication in juvenile rats: implications for mania models, Eur. Neuropsychopharmacol., 27, 261, 10.1016/j.euroneuro.2017.01.003 Burgdorf, 2001, Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats, Behav. Neurosci., 115, 940, 10.1037/0735-7044.115.4.940 Seffer, 2014, Pro-social ultrasonic communication in rats: insights from playback studies, J. Neurosci. Methods, 234, 73, 10.1016/j.jneumeth.2014.01.023 Wöhr, 2007, Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior?, PLoS One, 2, e1365, 10.1371/journal.pone.0001365 Sykes, 2018, Genetic variation in the psychiatric risk gene CACNA1C modulates reversal learning across species, Schizophr. Bull., 1–9 Braun, 2018, Sex-specific effects of Cacna1c haploinsufficiency on object recognition, spatial memory, and reversal learning capabilities in rats, Neurobiol. Learn. Mem., 155, 543, 10.1016/j.nlm.2018.05.012 Michels, 2018, Downregulation of the psychiatric susceptibility gene Cacna1c promotes mitochondrial resilience to oxidative stress in neuronal cells, Cell Death Discov., 4 Kisko, 2018, Cacna1c haploinsufficiency leads to pro-social 50-kHz ultrasonic communication deficits in rats, Dis. Model. Mech., 11, 10.1242/dmm.034116 Kisko, 2018, Sex-dependent effects of Cacna1c haploinsufficiency on juvenile social play behavior and pro-social 50-kHz ultrasonic communication in rats, Genes Brain Behav., e12552 Geurts, 2009, Knockout rats via embryo microinjection of zinc-finger nucleases, Science, 325, 10.1126/science.1172447 Wöhr, 2015, Critical involvement of 5-HT2C receptor function in amphetamine-induced 50-kHz ultrasonic vocalizations in rats, Psychopharmacology (Berl.), 232, 1817, 10.1007/s00213-014-3814-9 Pereira, 2014, Amphetamine-induced appetitive 50-kHz calls in rats: a marker of affect in mania?, Psychopharmacology (Berl.), 231, 2567, 10.1007/s00213-013-3413-1 Cohen, 1988 Burgdorf, 2008, Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback, J. Comp. Psychol., 122, 357, 10.1037/a0012889 Wright, 2010, Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context, Psychopharmacology (Berl.), 211, 1, 10.1007/s00213-010-1859-y Wöhr, 2018, Ultrasonic communication in rats: appetitive 50-kHz ultrasonic vocalizations as social contact calls, Behav. Ecol. Sociobiol. (Print), 72 Burgdorf, 2009, The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats, Dev. Psychobiol., 51, 34, 10.1002/dev.20343 Panksepp, 2001, Empathy and the action-perception resonances of basic socio-emotional systems of the brain, Behav. Brain Sci., 25, 43, 10.1017/S0140525X0247001X Kisko, 2015, Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization, Behav. Processes, 111, 25, 10.1016/j.beproc.2014.11.011 Burke, 2018, Do juvenile rats use specific ultrasonic calls to coordinate their social play?, Anim. Behav., 140, 81, 10.1016/j.anbehav.2018.03.019 Sungur, 2018, Impaired object recognition but normal social behavior and ultrasonic communication in Cofilin1 mutant mice, Front. Behav. Neurosci., 12, 1, 10.3389/fnbeh.2018.00025 Ferhat, 2016, Recording mouse ultrasonic vocalizations to evaluate social communication, J. Vis. Exp., 1 Burke, 2017, Avoiding escalation from play to aggression in adult male rats: the role of ultrasonic calls, Behav. Processes, 144, 72, 10.1016/j.beproc.2017.09.014 Ferdman, 2007, Weaning age, social isolation, and gender, interact to determine adult explorative and social behavior, and dendritic and spine morphology in prefrontal cortex of rats, Behav. Brain Res., 180, 174, 10.1016/j.bbr.2007.03.011 Snigdha, 2008, Efficacy of antipsychotics to reverse phencyclidine-induced social interaction deficits in female rats—a preliminary investigation, Behav. Brain Res., 187, 489, 10.1016/j.bbr.2007.10.012 Arakawa, 2010, Sickness-related odor communication signals as determinants of social behavior in rat: a role for inflammatory processes, Horm. Behav., 57, 330, 10.1016/j.yhbeh.2010.01.002 Zernig, 2015, Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor, Behav. Pharmacol., 26, 580, 10.1097/FBP.0000000000000167 Wang, 2011, Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex, Science, 334, 693, 10.1126/science.1209951 Saxena, 2018, Experiential contributions to social dominance in a rat model of fragile-X syndrome, Proc. R. Soc. B Biol. Sci., 285 Garfield, 2011, Distinct physiological and behavioural functions for parental alleles of imprinted Grb10, Nature, 469, 534, 10.1038/nature09651 Lenington, 1983, Social preferences for partners carrying ‘good genes’ in wild house mice, Anim. Behav., 31, 325, 10.1016/S0003-3472(83)80050-5 Wöhr, 2013, Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments, Behav. Brain Res., 251, 5, 10.1016/j.bbr.2013.05.047 Silverman, 2010, Behavioural phenotyping assays for mouse models of autism, Nat. Rev. Neurosci., 11, 490, 10.1038/nrn2851 Kalueff, 2016, Neurobiology of rodent self-grooming and its value for translational neuroscience, Nat. Rev. Neurosci., 17, 45, 10.1038/nrn.2015.8 Lee, 2012, Forebrain elimination of cacna1c mediates anxiety-like behavior in mice, Mol. Psychiatry, 17, 1054, 10.1038/mp.2012.71 Seisenberger, 2000, Functional embryonic cardiomyocytes after disruption of the L-type alpha1C (Cav1.2) calcium channel gene in the mouse, J. Biol. Chem., 275, 39193, 10.1074/jbc.M006467200 Becker, 2016, Female rats are not more variable than male rats: a meta-analysis of neuroscience studies, Biol. Sex Differ., 7, 34, 10.1186/s13293-016-0087-5 Strohmaier, 2013, The psychiatric vulnerability gene CACNA1C and its sex-specific relationship with personality traits, resilience factors and depressive symptoms in the general population, Mol. Psychiatry, 18, 607, 10.1038/mp.2012.53