The Amygdala Excitatory/Inhibitory Balance in a Valproate-Induced Rat Autism Model

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Lin, Hui Ching ^a   Gean, Po Wu ^b   Wang, Chao Chuan ^c   Chan, Yun Han ^b,d   Chen, Po See ^e,f  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d Center for Drug Evaluation   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^f NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AUTISM; BRAIN DEPTH RECORDING; BRAIN SLICE; CONDITIONING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MINIATURE ENDPLATE POTENTIAL; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PYRAMIDAL NERVE CELL; RAT; SOCIAL INTERACTION; SYNAPTIC TRANSMISSION; THALAMUS;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; AUTISTIC DISORDER; CONDITIONING, OPERANT; EXCITATORY POSTSYNAPTIC POTENTIALS; FEAR; HISTOLOGICAL TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL BEHAVIOR; SYNAPSES; VALPROIC ACID;

EID: 84873832901     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055248     Document Type: Article

References (75)

1. Adolphs R, Spezio M, (2006) Role of the amygdala in processing visual social stimuli. Prog Brain Res 156: 363-378.
2. Kuzmanovic B, Bente G, von Cramon DY, Schilbach L, Tittgemeyer M, et al. (2011) Imaging first impressions: Distinct neural processing of verbal and nonverbal social information. Neuroimage 60: 179-188.
3. LeDoux J, (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23: 727-738.
4. Amaral DG, (2002) The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol Psychiatry 51: 11-17.
5. Emery NJ, Capitanio JP, Mason WA, Machado CJ, Mendoza SP, et al. (2001) The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta). Behav Neurosci 115: 515-544.
6. LeDoux JE, (1995) Emotion: clues from the brain. Annu Rev Psychol 46: 209-235.
7. Markowitsch HJ, Staniloiu A, (2011) Amygdala in action: relaying biological and social significance to autobiographical memory. Neuropsychologia 49: 718-733.
8. Muscatell KA, Morelli SA, Falk EB, Way BM, Pfeifer JH, et al. (2012) Social status modulates neural activity in the mentalizing network. Neuroimage In press.
9. Bickart KC, Wright CI, Dautoff RJ, Dickerson BC, Barrett LF, (2011) Amygdala volume and social network size in humans. Nat Neurosci 14: 163-164.
10. Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, et al. (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474: 498-501.
11. Pejic T, Hermann A, Vaitl D, Stark R, (2011) Social anxiety modulates amygdala activation during social conditioning. Social Cognitive and Affective Neuroscience In press.
12. Baron-Cohen S, Ring HA, Bullmore ET, Wheelwright S, Ashwin C, et al. (2000) The amygdala theory of autism. Neurosci Biobehav Rev 24: 355-364.
13. Gadziola MA, Grimsley JM, Shanbhag SJ, Wenstrup JJ, (2012) A novel coding mechanism for social vocalizations in the lateral amygdala. J Neurophysiol 107: 1047-1057.
14. Saygin ZM, Osher DE, Augustinack J, Fischl B, Gabrieli JD, (2011) Connectivity-based segmentation of human amygdala nuclei using probabilistic tractography. Neuroimage 56: 1353-1361.
15. Becker B, Mihov Y, Scheele D, Kendrick KM, Feinstein JS, et al. (2012) Fear Processing and Social Networking in the Absence of a Functional Amygdala. Biol Psychiatry 72: 70-77.
16. Blair RJ, Peschardt KS, Budhani S, Mitchell DG, Pine DS, (2006) The development of psychopathy. J Child Psychol Psychiatry 47: 262-276.
17. Cottraux J, (2005) Recent developments in research and treatment for social phobia (social anxiety disorder). Curr Opin Psychiatry 18: 51-54.
18. Damsa C, Maris S, Pull CB, (2005) New fields of research in posttraumatic stress disorder: brain imaging. Curr Opin Psychiatry 18: 55-64.
19. Adolphs R, (2009) The social brain: neural basis of social knowledge. Annu Rev Psychol 60: 693-716.
20. Hampton AN, Adolphs R, Tyszka MJ, O'Doherty JP, (2007) Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron 55: 545-555.
21. Kennedy DP, Glascher J, Tyszka JM, Adolphs R, (2009) Personal space regulation by the human amygdala. Nat Neurosci 12: 1226-1227.
22. Tsuchiya N, Kawasaki H, Oya H, Howard MA 3rd, Adolphs R, (2008) Decoding face information in time, frequency and space from direct intracranial recordings of the human brain. PLoS One 3: e3892.
23. Heritch AJ, Henderson K, Westfall TC, (1990) Effects of social isolation on brain catecholamines and forced swimming in rats: prevention by antidepressant treatment. J Psychiatr Res 24: 251-258.
24. Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, et al. (1999) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11: 1891-1898.
25. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, et al. (2005) Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8: 519-526.
26. Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H, (2007) Abnormal activation of the social brain during face perception in autism. Hum Brain Mapp 28: 441-449.
27. Wang AT, Dapretto M, Hariri AR, Sigman M, Bookheimer SY, (2004) Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. J Am Acad Child Adolesc Psychiatry 43: 481-490.
28. Bailey A, Luthert P, Dean A, Harding B, Janota I, et al. (1998) A clinicopathological study of autism. Brain 121 (Pt 5):: 889-905.
29. Schumann CM, Amaral DG, (2006) Stereological analysis of amygdala neuron number in autism. J Neurosci 26: 7674-7679.
30. Aylward EH, Minshew NJ, Goldstein G, Honeycutt NA, Augustine AM, et al. (1999) MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology 53: 2145-2150.
31. Nacewicz BM, Dalton KM, Johnstone T, Long MT, McAuliff EM, et al. (2006) Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Arch Gen Psychiatry 63: 1417-1428.
32. Rojas DC, Smith JA, Benkers TL, Camou SL, Reite ML, et al. (2004) Hippocampus and amygdala volumes in parents of children with autistic disorder. Am J Psychiatry 161: 2038-2044.
33. Todd RM, Anderson AK, (2009) Six degrees of separation: the amygdala regulates social behavior and perception. Nat Neurosci 12: 1217-1218.
34. Silverman JL, Yang M, Lord C, Crawley JN, (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11: 490-502.
35. Rinaldi T, Silberberg G, Markram H, (2008) Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18: 763-770.
36. 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.
37. Genton P, Semah F, Trinka E, (2006) Valproic acid in epilepsy: pregnancy-related issues. Drug Saf 29: 1-21.
38. 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.
39. Rasalam AD, Hailey H, Williams JH, Moore SJ, Turnpenny PD, et al. (2005) Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev Med Child Neurol 47: 551-555.
40. Schneider T, Przewlocki R, (2005) Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30: 80-89.
41. Schneider T, Ziolkowska B, Gieryk A, Tyminska A, Przewlocki R, (2007) Prenatal exposure to valproic acid disturbs the enkephalinergic system functioning, basal hedonic tone, and emotional responses in an animal model of autism. Psychopharmacology (Berl) 193: 547-555.
42. 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.
43. Chiao JY, Iidaka T, Gordon HL, Nogawa J, Bar M, et al. (2008) Cultural specificity in amygdala response to fear faces. J Cogn Neurosci 20: 2167-2174.
44. McRae K, Gross JJ, Weber J, Robertson ER, Sokol-Hessner P, et al. (2012) The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc Cogn Affect Neurosci 7: 11-22.
45. Keightley ML, Chiew KS, Winocur G, Grady CL, (2007) Age-related differences in brain activity underlying identification of emotional expressions in faces. Soc Cogn Affect Neurosci 2: 292-302.
46. Flagstad P, Mork A, Glenthoj BY, van Beek J, Michael-Titus AT, et al. (2004) Disruption of neurogenesis on gestational day 17 in the rat causes behavioral changes relevant to positive and negative schizophrenia symptoms and alters amphetamine-induced dopamine release in nucleus accumbens. Neuropsychopharmacology 29: 2052-2064.
47. Lin HC, Tseng YC, Mao SC, Chen PS, Gean PW, (2011) GABAA receptor endocytosis in the basolateral amygdala is critical to the reinstatement of fear memory measured by fear-potentiated startle. J Neurosci 31: 8851-8861.
48. Yu SY, Wu DC, Liu L, Ge Y, Wang YT, (2008) Role of AMPA receptor trafficking in NMDA receptor-dependent synaptic plasticity in the rat lateral amygdala. J Neurochem 106: 889-899.
49. Washburn MS, Moises HC, (1992) Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro. J Neurosci 12: 4066-4079.
50. Evans DW, Canavera K, Kleinpeter FL, Maccubbin E, Taga K, (2005) The fears, phobias and anxieties of children with autism spectrum disorders and Down syndrome: comparisons with developmentally and chronologically age matched children. Child Psychiatry Hum Dev 36: 3-26.
51. Barad M, Gean PW, Lutz B, (2006) The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60: 322-328.
52. Hess G, Kuhnt U, Voronin LL, (1987) Quantal analysis of paired-pulse facilitation in guinea pig hippocampal slices. Neurosci Lett 77: 187-192.
53. Lin HC, Mao SC, Su CL, Gean PW, (2010) Alterations of excitatory transmission in the lateral amygdala during expression and extinction of fear memory. Int J Neuropsychopharmacol 13: 335-345.
54. Bellone C, Luscher C, (2006) Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat Neurosci 9: 636-641.
55. Clem RL, Barth A, (2006) Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49: 663-670.
56. Du J, Creson TK, Wu LJ, Ren M, Gray NA, et al. (2008) The role of hippocampal GluR1 and GluR2 receptors in manic-like behavior. J Neurosci 28: 68-79.
57. Schneider T, Roman A, Basta-Kaim A, Kubera M, Budziszewska B, et al. (2008) Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid. Psychoneuroendocrinology 33: 728-740.
58. Iwasaki-Sekino A, Mano-Otagiri A, Ohata H, Yamauchi N, Shibasaki T, (2009) Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 34: 226-237.
59. Kataoka S, Takuma K, Hara Y, Maeda Y, Ago Y, et al. (2011) Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid. Int J Neuropsychopharmacol In press.
60. Bachevalier J, Loveland KA, (2006) The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neurosci Biobehav Rev 30: 97-117.
61. Kleinhans NM, Richards T, Weaver K, Johnson LC, Greenson J, et al. (2010) Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders. Neuropsychologia 48: 3665-3670.
62. 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.
63. Rubenstein JL, Merzenich MM, (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior 2: 255-267.
64. Whalley K, (2012) Neurodevelopmental disorders: a fragile synaptic balance. Nat Rev Neurosci 13: 3.
65. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, et al. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477: 171-178.
66. 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.
67. Marin O, (2012) Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13: 107-120.
68. Nelson ED, Bal M, Kavalali ET, Monteggia LM, (2011) Selective impact of MeCP2 and associated histone deacetylases on the dynamics of evoked excitatory neurotransmission. J Neurophysiol 106: 193-201.
69. Barrow SL, Constable JR, Clark E, El-Sabeawy F, McAllister AK, et al. (2009) Neuroligin1: a cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Development 4: 17.
70. Craig AM, Kang Y, (2007) Neurexin-neuroligin signaling in synapse development. Curr Opin Neurobiol 17: 43-52.
71. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T, (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101: 657-669.
72. Jung SY, Kim J, Kwon OB, Jung JH, An K, et al. (2010) Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors. Proc Natl Acad Sci U S A 107: 4710-4715.
73. Blundell J, Blaiss CA, Etherton MR, Espinosa F, Tabuchi K, et al. (2010) Neuroligin-1 deletion results in impaired spatial memory and increased repetitive behavior. J Neurosci 30: 2115-2129.
74. Etherton MR, Tabuchi K, Sharma M, Ko J, Sudhof TC, (2011) An autism-associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor-mediated synaptic transmission in hippocampus. EMBO J 30: 2908-2919.
75. Sudhof TC, (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911.