Gestational valproate alters BOLD activation in response to complex social and primary sensory stimuli

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Felix Ortiz, Ada C ^a   Febo, Marcelo ^a,b  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VALPROIC ACID; VASOPRESSIN RECEPTOR ANTAGONIST; VASOPRESSIN V1A RECEPTOR; ARGIPRESSIN; DRUG DERIVATIVE; OXYGEN; VASOPRESSIN RECEPTOR; VASOPRESSIN, 1 (1 MERCAPTOCYCLOHEXANEACETIC ACID) 2 (O METHYL L TYROSINE) 8 L ARGININE; VASOPRESSIN, 1-(1-MERCAPTOCYCLOHEXANEACETIC ACID)-2-(O- METHYL-L-TYROSINE)-8-L-ARGININE-;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GESTATIONAL AGE; GROOMING; HYPOTHALAMUS; IMAGE ANALYSIS; LOCOMOTION; MESENCEPHALON; NEUROIMAGING; NEUROTRANSMISSION; NONHUMAN; RAT; RECEPTOR BLOCKING; SENSORY STIMULATION; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STIMULUS RESPONSE; TEMPORAL CORTEX; THALAMUS; VISUAL STIMULATION; ANIMAL; BLOOD; DRUG ANTAGONISM; DRUG EFFECT; MALE; MOTOR ACTIVITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; VISION; VOCALIZATION;

ANIMALIA; RATTUS;

ANIMALS; ARGININE VASOPRESSIN; BEHAVIOR, ANIMAL; FEMALE; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; OXYGEN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, VASOPRESSIN; SOCIAL BEHAVIOR; VALPROIC ACID; VISION, OCULAR; VOCALIZATION, ANIMAL;

EID: 84861203989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037313     Document Type: Article

References (51)

1. Abrahams BS, Geschwind DH, (2008) Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 9: 341-355.
2. Kim SJ, Young LJ, Gonen D, Veenstra-VanderWeele J, Courchesne R, et al. (2002) Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 7: 503-507.
3. Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ, (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29: 483-493.
4. Israel S, Lerer E, Shalev I, Uzefovsky F, Reibold M, et al. (2008) Molecular genetic studies of the arginine vasopressin 1a receptor (AVPR1a) and the oxytocin receptor (OXTR) in human behaviour: from autism to altruism with some notes in between. Prog Brain Res 170: 435-449.
5. Christianson AL, Chesler N, Kromberg JG, (1994) Fetal valproate syndrome: clinical and neuro-developmental features in two sibling pairs. Dev Med Child Neurol 36: 361-369.
6. Hellings JA, Nickel EJ, Weckbaugh M, McCarter K, Mosier M, et al. (2005) The overt aggression scale for rating aggression in outpatient youth with autistic disorder: preliminary findings. J Neuropsychiatry Clin Neurosci 17: 29-35.
7. Moore SJ, Turnpenny P, Quinn A, Glover S, Lloyd DJ, et al. (2000) A clinical study of 57 children with fetal anticonvulsant syndromes. J Med Genet 37: 489-497.
8. Williams G, King J, Cunningham M, Stephan M, Kerr B, et al. (2001) Fetal valproate syndrome and autism: additional evidence of an association. Dev Med Child Neurol 43: 202-206.
9. Arndt TL, Stodgell CJ, Rodier PM, (2005) The teratology of autism. Int J Dev Neurosci 23: 189-199.
10. Schneider T, Przewlocki R, (2005) Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30: 80-89.
11. Wagner GC, Reuhl KR, Cheh M, McRae P, Halladay AK, (2006) A new neurobehavioral model of autism in mice: pre- and postnatal exposure to sodium valproate. J Autism Dev Disord 36: 779-793.
12. Stodgell CJ, Ingram JL, O'Bara M, Tisdale BK, Nau H, et al. (2006) Induction of the homeotic gene Hoxa1 through valproic acid's teratogenic mechanism of action. Neurotoxicol Teratol 28: 617-624.
13. Miyazaki K, Narita N, Narita M, (2005) Maternal administration of thalidomide or valproic acid causes abnormal serotonergic neurons in the offspring: implication for pathogenesis of autism. Int J Dev Neurosci 23: 287-297.
14. Rodier PM, Ingram JL, Tisdale B, Nelson S, Romano J, (1996) Embryological origin for autism: developmental anomalies of the cranial nerve motor nuclei. J Comp Neurol 370: 247-261.
15. Markram K, Rinaldi T, La Mendola D, Sandi C, Markram H, (2008) Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 33: 901-912.
16. Schneider T, Labuz D, Przewlocki R, (2001) Nociceptive changes in rats after prenatal exposure to valproic acid. Pol J Pharmacol 53: 531-534.
17. Ingram JL, Peckham SM, Tisdale B, Rodier PM, (2000) Prenatal exposure of rats to valproic acid reproduces the cerebellar anomalies associated with autism. Neurotoxicol Teratol 22: 319-324.
18. Rinaldi T, Silberberg G, Markram H, (2008) Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18: 763-770.
19. Ostrowski NL, Lolait SJ, Young WS, 3rd, (1994) Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. Endocrinology 135: 1511-1528.
20. Murray EK, Varnum MM, Fernandez JL, de Vries GJ, Forger NG, (2011) Effects of neonatal treatment with valproic acid on vasopressin immunoreactivity and olfactory behaviour in mice. J Neuroendocrinol 23: 906-914.
21. Ehret G, (2005) Infant rodent ultrasounds: a gate to the understanding of sound communication. Behav Genet 35: 19-29.
22. Walcott EC, Higgins EA, Desai NS, (2011) Synaptic and intrinsic balancing during postnatal development in rat pups exposed to valproic acid in utero. J Neurosci 31: 13097-13109.
23. Markram H, Rinaldi T, Markram K, (2007) The intense world syndrome-an alternative hypothesis for autism. Front Neurosci 1: 77-96.
24. Rinaldi T, Kulangara K, Antoniello K, Markram H, (2007) Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc Natl Acad Sci U S A 104: 13501-13506.
25. Rinaldi T, Perrodin C, Markram H, (2008) Hyper-connectivity and hyper-plasticity in the medial prefrontal cortex in the valproic Acid animal model of autism. Front Neural Circuits 2: 4.
26. LeDoux JE, (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
27. Cohen ER, Ugurbil K, Kim SG, (2002) Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J Cereb Blood Flow Metab 22: 1042-1053.
28. Hyder F, Rothman DL, Shulman RG, (2002) Total neuroenergetics support localized brain activity: implications for the interpretation of fMRI. Proc Natl Acad Sci U S A 99: 10771-10776.
29. Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, et al. (2002) Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc Natl Acad Sci U S A 99: 10765-10770.
30. Knafo A, Israel S, Darvasi A, Bachner-Melman R, Uzefovsky F, et al. (2008) Individual differences in allocation of funds in the dictator game associated with length of the arginine vasopressin 1a receptor RS3 promoter region and correlation between RS3 length and hippocampal mRNA. Genes Brain Behav 7: 266-275.
31. Yirmiya N, Rosenberg C, Levi S, Salomon S, Shulman C, et al. (2006) Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Mol Psychiatry 11: 488-494.
32. Donaldson ZR, Kondrashov FA, Putnam A, Bai Y, Stoinski TL, et al. (2008) Evolution of a behavior-linked microsatellite-containing element in the 5′ flanking region of the primate AVPR1A gene. BMC Evol Biol 8: 180.
33. Hammock EA, Lim MM, Nair HP, Young LJ, (2005) Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes Brain Behav 4: 289-301.
34. Egashira N, Tanoue A, Matsuda T, Koushi E, Harada S, et al. (2007) Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav Brain Res 178: 123-127.
35. Murgatroyd C, Wigger A, Frank E, Singewald N, Bunck M, et al. (2004) Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J Neurosci 24: 7762-7770.
36. Wigger A, Sanchez MM, Mathys KC, Ebner K, Frank E, et al. (2004) Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29: 1-14.
37. Caffrey MK, Nephew BC, Febo M, (2010) Central vasopressin V1a receptors modulate neural processing in mothers facing intruder threat to pups. Neuropharmacology 58: 107-116.
38. Brudzynski SM, Kehoe P, Callahan M, (1999) Sonographic structure of isolation-induced ultrasonic calls of rat pups. Dev Psychobiol 34: 195-204.
39. Zeskind PS, McMurray MS, Garber KA, Neuspiel JM, Cox ET, et al. (2011) Development of translational methods in spectral analysis of human infant crying and rat pup ultrasonic vocalizations for early neurobehavioral assessment. Front Psychiatry 2: 56.
40. Branchi I, Santucci D, Vitale A, Alleva E, (1998) Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Dev Psychobiol 33: 249-256.
41. Brudzynski SM, Barnabi F, (1996) Contribution of the ascending cholinergic pathways in the production of ultrasonic vocalization in the rat. Behav Brain Res 80: 145-152.
42. Panksepp JB, Jochman KA, Kim JU, Koy JJ, Wilson ED, et al. (2007) Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS One 2: e351.
43. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN, (2008) Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One 3: e3067.
44. Veenema AH, Neumann ID, (2009) Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34: 463-467.
45. Ennaceur A, Neave N, Aggleton JP, (1997) Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113: 509-519.
46. King JA, Garelick TS, Brevard ME, Chen W, Messenger TL, et al. (2005) Procedure for minimizing stress for fMRI studies in conscious rats. J Neurosci Methods 148: 154-160.
47. Ferris CF, Kulkarni P, Sullivan JM Jr, Harder JA, Messenger TL, et al. (2005) Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25: 149-156.
48. Ferris CF, Stolberg T, Kulkarni P, Murugavel M, Blanchard R, et al. (2008) Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neurosci 9: 111.
49. Febo M, Segarra AC, Tenney JR, Brevard ME, Duong TQ, et al. (2004) Imaging cocaine-induced changes in the mesocorticolimbic dopaminergic system of conscious rats. J Neurosci Methods 139: 167-176.
50. Nephew BC, Caffrey MK, Felix-Ortiz AC, Ferris CF, Febo M, (2009) Blood oxygen level-dependent signal responses in corticolimbic 'emotions' circuitry of lactating rats facing intruder threat to pups. Eur J Neurosci 30: 934-945.
51. Genovese CR, Lazar NA, Nichols T, (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15: 870-878.