Behavioral training reverses global cortical network dysfunction induced by perinatal antidepressant exposure

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 7, 2015, Pages 2233-2238

  Zhou, Xiaoming ^a,b   Lu, Jordan Y F ^c   Darling, Ryan D ^c   Simpson, Kimberly L ^c   Zhu, Xiaoqing ^a   Wang, Fang ^a   Yu, Liping ^a   Sun, Xinde ^a   Merzenich, Michael M ^c   Lin, Rick C S ^c,d  

^a B326 Science Building   (China)

^b NEW YORK UNIVERSITY SHANGHAI   (China)

^c UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antidepressant exposure; Autism; Behavioral training; Cortical network; Recovery of function

Indexed keywords

ANTIDEPRESSANT AGENT; CITALOPRAM; SEROTONIN UPTAKE INHIBITOR;

ANIMAL EXPERIMENT; ARTICLE; AUTISM; BEHAVIOR; BRAIN CORTEX; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG EXPOSURE; FEMALE; INTERNEURON; MALE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; ANIMAL; ANIMAL BEHAVIOR; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SPRAGUE DAWLEY RAT;

RATTUS; RODENTIA;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; FEMALE; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN UPTAKE INHIBITORS;

EID: 84923283147     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416582111     Document Type: Article

References (48)

1. Arndt TL, Stodgell CJ, Rodier PM (2005) The teratology of autism. Int J Dev Neurosci 23(2-3):189-199.
2. Geschwind DH, Levitt P (2007) Autism spectrum disorders: Developmental disconnection syndromes. Curr Opin Neurobiol 17(1):103-111.
3. Geschwind DH (2008) Autism: Family connections. Nature 454(7206):838-839.
4. Schaaf CP, Zoghbi HY (2011) Solving the autism puzzle a few pieces at a time. Neuron 70(5):806-808.
5. State MW, Sestan N (2012) Neuroscience. The emerging biology of autism spectrum disorders. Science 337(6100):1301-1303.
6. Bethea TC, Sikich L (2007) Early pharmacological treatment of autism: A rationale for developmental treatment. Biol Psychiatry 61(4):521-537.
7. King BH, et al.; STAART Psychopharmacology Network (2009) Lack of efficacy of citalopram in children with autism spectrum disorders and high levels of repetitive behavior: Citalopram ineffective in children with autism. Arch Gen Psychiatry 66(6): 583-590.
8. West L, Brunssen SH, Waldrop J (2009) Review of the evidence for treatment of children with autism with selective serotonin reuptake inhibitors. J Spec Pediatr Nurs 14(3):183-191.
9. Carrasco M, Volkmar FR, Bloch MH (2012) Pharmacologic treatment of repetitive behaviors in autism spectrum disorders: Evidence of publication bias. Pediatrics 129(5):e1301-e1310.
10. Dawson G, et al. (2010) Randomized, controlled trial of an intervention for toddlers with autism: The Early Start Denver Model. Pediatrics 125(1):e17-e23.
11. Fein D, et al. (2013) Optimal outcome in individuals with a history of autism. J Child Psychol Psychiatry 54(2):195-205.
12. Rubenstein JL, Merzenich MM (2003) Model of autism: Increased ratio of excitation/ inhibition in key neural systems. Genes Brain Behav 2(5):255-267.
13. DiCicco-Bloom E, et al. (2006) The developmental neurobiology of autism spectrum disorder. J Neurosci 26(26):6897-6906.
14. Zikopoulos B, Barbas H (2010) Changes in prefrontal axons may disrupt the network in autism. J Neurosci 30(44):14595-14609.
15. Shukla DK, Keehn B, Smylie DM, Müller RA (2011) Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia 49(5):1378-1382.
16. Dinstein I, et al. (2011) Disrupted neural synchronization in toddlers with autism. Neuron 70(6):1218-1225.
17. Gkogkas CG, et al. (2013) Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493(7432):371-377.
18. Homberg JR, Schubert D, Gaspar P (2010) New perspectives on the neurodevelopmental effects of SSRIs. Trends Pharmacol Sci 31(2):60-65.
19. Maciag D, et al. (2006) Neonatal antidepressant exposure has lasting effects on behavior and serotonin circuitry. Neuropsychopharmacology 31(1):47-57.
20. Simpson KL, et al. (2011) Perinatal antidepressant exposure alters cortical network function in rodents. Proc Natl Acad Sci USA 108(45):18465-18470.
21. Weikum WM, Oberlander TF, Hensch TK, Werker JF (2012) Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proc Natl Acad Sci USA 109(Suppl 2):17221-17227.
22. Harrington RA, Lee LC, Crum RM, Zimmerman AW, Hertz-Picciotto I (2014) Prenatal SSRI use and offspring with autism spectrum disorder or developmental delay. Pediatrics 133(5):e1241-e1248.
23. Oram Cardy JE, Flagg EJ, Roberts W, Brian J, Roberts TP (2005) Magnetoencephalography identifies rapid temporal processing deficit in autism and language impairment. Neuroreport 16(4):329-332.
24. Bao S, Chang EF, Davis JD, Gobeske KT, Merzenich MM (2003) Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J Neurosci 23(34):10765-10775.
25. Zhou X, Merzenich MM (2007) Intensive training in adults refines A1 representations degraded in an early postnatal critical period. Proc Natl Acad Sci USA 104(40): 15935-15940.
26. Zhou X, Merzenich MM (2009) Developmentally degraded cortical temporal processing restored by training. Nat Neurosci 12(1):26-28.
27. de Villers-Sidani E, et al. (2010) Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proc Natl Acad Sci USA 107(31):13900-13905.
28. Greenshaw AJ (2003) Neurotransmitter interactions in psychotropic drug action: Beyond dopamine and serotonin. J Psychiatry Neurosci 28(4):247-250.
29. Vasudeva RK, Lin RC, Simpson KL, Waterhouse BD (2011) Functional organization of the dorsal raphe efferent system with special consideration of nitrergic cell groups. J Chem Neuroanat 41(4):281-293.
30. Zhou FM, et al. (2005) Corelease of dopamine and serotonin from striatal dopamine terminals. Neuron 46(1):65-74.
31. Cases O, et al. (1998) Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs. J Neurosci 18(17):6914-6927.
32. Zhou FC, Lesch KP, Murphy DL (2002) Serotonin uptake into dopamine neurons via dopamine transporters: A compensatory alternative. Brain Res 942(1-2):109-119.
33. Narboux-Nême N, Pavone LM, Avallone L, Zhuang X, Gaspar P (2008) Serotonin transporter transgenic (SERTcre) mouse line reveals developmental targets of serotonin specific reuptake inhibitors (SSRIs). Neuropharmacology 55(6):994-1005.
34. Berridge CW, Waterhouse BD (2003) The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42(1):33-84.
35. Oberlander TF, et al. (2005) Pain reactivity in 2-month-old infants after prenatal and postnatal serotonin reuptake inhibitor medication exposure. Pediatrics 115(2): 411-425.
36. Rogers SJ, Ozonoff S (2005) Annotation: What do we know about sensory dysfunction in autism? A critical review of the empirical evidence. J Child Psychol Psychiatry 46(12):1255-1268.
37. Bennetto L, Kuschner ES, Hyman SL (2007) Olfaction and taste processing in autism. Biol Psychiatry 62(9):1015-1021.
38. Schmitz C, et al. (2005) Autism: Neuropathology, alterations of the GABAergic system, and animal models. Int Rev Neurobiol 71:1-26.
39. Blatt GJ, Fatemi SH (2011) Alterations in GABAergic biomarkers in the autism brain: Research findings and clinical implications. Anat Rec (Hoboken) 294(10):1646-1652.
40. Khan S, et al. (2013) Local and long-range functional connectivity is reduced in concert in autism spectrum disorders. Proc Natl Acad Sci USA 110(8):3107-3112.
41. Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3(9):904-910.
42. Gao WJ, Wormington AB, Newman DE, Pallas SL (2000) Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: Immunocytochemical localization of calbindin-and parvalbumin-containing neurons. J Comp Neurol 422: 140-157.
43. de Villers-Sidani E, Simpson KL, Lu YF, Lin RC, Merzenich MM (2008) Manipulating critical period closure across different sectors of the primary auditory cortex. Nat Neurosci 11(8):957-965.
44. Zhou X, Merzenich MM (2012) Environmental noise exposure degrades normal listening processes. Nat Commun 3:843.
45. Darling RD, et al. (2011) Perinatal citalopram exposure selectively increases locus ceruleus circuit function in male rats. J Neurosci 31(46):16709-16715.
46. Zhang J, et al. (2013) Neonatal citalopram exposure decreases serotonergic fiber density in the olfactory bulb of male but not female adult rats. Front Cell Neurosci 7:67.
47. Fernell E, et al. (2010) Developmental profiles in preschool children with autism spectrum disorders referred for intervention. Res Dev Disabil 31(3):790-799.
48. Moore AK, Wehr M (2013) Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci 33(34):13713-13723.