Prenatal drug exposure affects neonatal brain functional connectivity

Journal of Neuroscience

Volumn 35, Issue 14, 2015, Pages 5860-5869

  Salzwedel, Andrew P ^a   Grewen, Karen M ^a   Vachet, Clement ^b   Gerig, Guido ^b   Lin, Weili ^a   Gao, Wei ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Amygdala; FMRI; Functional connectivity; Infant; Insula; Prenatal drug exposure

Indexed keywords

ALCOHOL; COCAINE; NICOTINE; ALCOHOL DERIVATIVE; CANNABIS; OXYGEN;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; CANNABIS SMOKING; CONNECTOME; CONTROLLED STUDY; EDINBURGH POSTNATAL DEPRESSION SCALE; EDUCATIONAL STATUS; ENVIRONMENTAL FACTOR; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GESTATIONAL AGE; HUMAN; INFANT; INSULA; MAJOR CLINICAL STUDY; MALE; NERVE CELL DIFFERENTIATION; NEUROLOGIC EXAMINATION; PREFRONTAL CORTEX; PREGNANT WOMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PUERPERAL DEPRESSION; SLEEP AROUSAL DISORDER; ANALYSIS OF VARIANCE; BLOOD; BRAIN; BRAIN MAPPING; IMAGE PROCESSING; MOVEMENT (PHYSIOLOGY); NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; VASCULARIZATION;

ALCOHOLS; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CANNABIS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT; MAGNETIC RESONANCE IMAGING; MALE; MOVEMENT; NEURAL PATHWAYS; NICOTINE; OXYGEN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84929380144     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4333-14.2015     Document Type: Article

References (80)

1. Adinoff B (2004) Neurobiologic processes in drug reward and addiction. Harv Rev Psychiatry 12:305–320.
2. Afif A, Bouvier R, Buenerd A, Trouillas J, Mertens P (2007) Development of the human fetal insular cortex: study of the gyration from 13 to 28 gestational weeks. Brain Struct Funct 212:335–346.
3. Alcauter S, Lin W, Keith Smith J, Gilmore JH, Gao W (2013) Consistent anterior-posterior segregation of the insula during the first 2 years of life. Cereb Cortex. Advance online publication. Retrieved March 10, 2015. 10.1093/cercor/bht312.
4. Alcauter S, Lin W, Smith JK, Short SJ, Goldman BD, Reznick JS, Gilmore JH, Gao W (2014) Development of thalamocortical connectivity during in fancy and its cognitive correlations. J Neurosci 34:9067–9075.
5. Baas D, Aleman A, Kahn RS (2004) Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res Brain Res Rev 45:96–103.
6. Bard KA, Coles CD, Platzman KA, Lynch ME (2000) The effects of prenatal drug exposure, term status, and caregiving on arousal and arousal modulation in 8-week-old infants. Dev Psychobiol 36:194–212.
7. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Statist 29:1165–1188.
8. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541.
9. Cauda F, Cavanna AE, D’agata F, Sacco K, Duca S, Geminiani GC (2011) Functional connectivity and coactivation of the nucleus accumbens: a combined functional connectivity and structure-based meta-analysis. J Cogn Neurosci 23:2864–2877.
10. Chen G, Adleman NE, Saad ZS, Leibenluft E, Cox RW (2014) Applications of multivariate modeling to neuroimaging group analysis: a comprehensive alternative to univariate general linear model. Neuroimage 99:571– 588.
11. Cho YT, Fromm S, Guyer AE, Detloff A, Pine DS, Fudge JL, Ernst M (2013) Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents. Neuroimage 66:508–521.
12. Cisler JM, Elton A, Kennedy AP, Young J, Smitherman S, Andrew James G, Kilts CD (2013) Altered functional connectivity of the insular cortex across prefrontal networks in cocaine addiction. Psychiatry Res 213:39–46.
13. Coles CD, Bard KA, Platzman KA, Lynch ME (1999) Attentional response at eight weeks in prenatally drug-exposed and preterm infants. Neurotoxicol Teratol 21:527–537.
14. Covert RF, Schreiber MD, Tebbett IR, Torgerson LJ (1994) Hemodynamic and cerebral blood flow effects of cocaine, cocethylene and benzoylecgonine in consious and anesthetized fetal lambs. J Pharmacol Exp Ther 270:118–126.
15. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173.
16. Craig ADB (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571.
17. Crandall JE, McCarthy DM, Araki KY, Sims JR, Ren JQ, Bhide PG (2007) Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J Neurosci 27:3813–3822.
18. Derauf C, Kekatpure M, Neyzi N, Lester B, Kosofsky B (2009) Neuroimaging of children following prenatal drug exposure. Semin Cell Dev Biol 20:441–454.
19. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968– 980.
20. Doria V, Beckmann CF, Arichi T, Merchant N, Groppo M, Turkheimer FE, Counsell SJ, Murgasova M, Aljabar P, Nunes RG, Larkman DJ, Rees G, Edwards AD (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci U S A 107:20015–20020.
21. Dow-Edwards DL, Benveniste H, Behnke M, Bandstra ES, Singer LT, Hurd YL, Stanford LR (2006) Neuroimaging of prenatal drug exposure. Neurotoxicol Teratol 28:386–402.
22. Eiden RD, McAuliffe S, Kachadourian L, Coles C, Colder C, Schuetze P (2009) Effects of prenatal cocaine exposure on infant reactivity and regulation. Neurotoxicol Teratol 31:60–68.
23. Eiden RD, Godleski S, Colder CR, Schuetze P (2014) Prenatal cocaine exposure: the role of cumulative environmental risk and maternal harshness in the development of child internalizing behavior problems in kindergarten. Neurotoxicol Teratol 44:1–10.
24. Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE (2009) Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol 5:e1000381.
25. Fallone MD, LaGasse LL, Lester BM, Shankaran S, Bada HS, Bauer CR (2014) Reactivity and regulation of motor responses in cocaine-exposed infants. Neurotoxicol Teratol 43:25–32.
26. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636–647.
27. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673–9678.
28. Fransson P, Aden U, Blennow M, Lagercrantz H (2011) The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex 21:145–154.
29. Gao W, Lin W (2012) Frontal parietal control network regulates the anticorrelated default and dorsal attention networks. Hum Brain Mapp 33: 192–202.
30. Gao W, Zhu H, Giovanello KS, Smith JK, Shen D, Gilmore JH, Lin W (2009) Evidence on the emergence of the brain’s default network from 2-weekold to 2-year-old healthy pediatric subjects. Proc Natl Acad Sci U S A 106:6790–6795.
31. Gao W, Gilmore JH, Giovanello KS, Smith JK, Shen D, Zhu H, Lin W (2011) Temporal and spatial evolution of brain network topology during the first two years of life. PLoS One 6:e25278.
32. Gao W, Gilmore JH, Shen D, Smith JK, Zhu H, Lin W (2013) The synchronization within and interaction between the default and dorsal attention networks in early infancy. Cereb Cortex 23:594–603.
33. Gao W, Elton A, Zhu H, Alcauter S, Smith JK, Gilmore JH, Lin W (2014a) Intersubject variability of and genetic effects on the brain’s functional connectivity during infancy. J Neurosci 34:11288–11296.
34. Gao W, Alcauter S, Elton A, Hernandez-Castillo CR, Smith JK, Ramirez J, Lin W (2014b) Functional network development during the first year: relative sequence and socioeconomic correlations. Cereb Cortex. Advance online publication. Retrieved March 10, 2015. doi:10.1093/cercor/ bhu088.
35. Gao W, Alcauter S, Smith JK, Gilmore JH, Lin W (2015) Development of human brain cortical network architecture during infancy. Brain Struct Funct 220:1173–1186.
36. Gee DG, Karlsgodt KH, van Erp TGM, Bearden CE, Lieberman MD, Belger A, Perkins DO, Olvet DM, Cornblatt BA, Constable T, Woods SW, Addington J, Cadenhead KS, McGlashan TH, Seidman LJ, Tsuang MT, Walker EF, Cannon TD (2012) Altered age-related trajectories of amygdalaprefrontal circuitry in adolescents at clinical high risk for psychosis: a preliminary study. Schizophr Res 134:1–9.
37. Grewen K, Burchinal M, Vachet C, Gouttard S, Gilmore JH, Lin W, Johns J, Elam M, Gerig G (2014) Prenatal cocaine effects on brain structure in early infancy. Neuroimage 101:114–123.
38. Gu H, Salmeron BJ, Ross TJ, Geng X, Zhan W, Stein EA, Yang Y (2010) Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage 53:593– 601.
39. Harrison NA, Gray MA, Gianaros PJ, Critchley HD (2010) The embodiment of emotional feelings in the brain. J Neurosci 30:12878–12884.
40. Hurt H, Giannetta JM, Korczykowski M, Hoang A, Tang KZ, Betancourt L, Brodsky NL, Shera DM, Farah MJ, Detre JA (2008) Functional magnetic resonance imaging and working memory in adolescents with gestational cocaine exposure. J Pediatr 152:371–377.
41. Ibañez A, Gleichgerrcht E, Manes F (2010) Clinical effects of insular damage in humans. Brain Struct Funct 214:397–410.
42. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) Fsl. Neuroimage 62:782–790.
43. Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2008) Competition between functional brain networks mediates behavioral variability. Neuroimage 39:527–537.
44. Knutson B, Greer SM (2008) Anticipatory affect: neural correlates and consequences for choice. Philos Trans R Soc Lond B Biol Sci 363:3771–3786.
45. Lambert BL, Bauer CR (2012) Developmental and behavioral consequences of prenatal cocaine exposure: a review. J Perinatol 32:819–828.
46. Lester BM, Tronick EZ, LaGasse L, Seifer R, Bauer CR, Shankaran S, Bada HS, Wright LL, Smeriglio VL, Lu J, Finnegan LP, Maza PL (2002) The maternal lifestyle study: effects of substance exposure during pregnancy on neurodevelopmental outcome in 1-month-old infants. Pediatrics 110: 1182–1192.
47. Lester BM, Lagasse L, Seifer R, Tronick EZ, Bauer CR, Shankaran S, Bada HS, Wright LL, Smeriglio VL, Liu J, Finnegan LP, Maza PL (2003) The Maternal Lifestyle Study (MLS): effects of prenatal cocaine and/or opiate exposure on auditory brain response at one month. J Pediatr 142:279– 285.
48. Li Z, Coles CD, Lynch ME, Hamann S, Peltier S, LaConte S, Hu X (2009) Prenatal cocaine exposure alters emotional arousal regulation and its effects on working memory. Neurotoxicol Teratol 31:342–348.
49. Li Z, Santhanam P, Coles CD, Lynch ME, Hamann S, Peltier S, Hu X (2011) Increased “default mode” activity in adolescents prenatally exposed to cocaine. Hum Brain Mapp 32:759–770.
50. Li Z, Santhanam P, Coles CD, Ellen Lynch M, Hamann S, Peltier S, Hu X (2013) Prenatal cocaine exposure alters functional activation in the ventral prefrontal cortex and its structural connectivity with the amygdala. Psychiatry Res 213:47–55.
51. Liu X, Hairston J, Schrier M, Fan J (2011) Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 35:1219–1236.
52. Mayes LC (2002) A behavioral teratogenic model of the impact of prenatal cocaine exposure on arousal regulatory systems. Neurotoxicol Teratol 24:385–395.
53. Mayes LC (2006) Arousal regulation, emotional flexibility, medial amygdala function, and the impact of early experience: comments on the paper of Lewis et al. Ann NY Acad Sci 1094:178–192.
54. McHugh MJ, Demers CH, Braud J, Briggs R, Adinoff B, Stein EA (2013) Striatal-insula circuits in cocaine addiction: implications for impulsivity and relapse risk. Am J Drug Alcohol Abuse 39:424–432.
55. Meyer JS, Quenzer LF (2005) Psychopharmacology: drugs, the brain, and behavior. Sunderland, MA: Sinauer.
56. Morrow CE, Bandstra ES, Anthony JC, Ofir AY, Xue L, Reyes ML (2001) Influence of prenatal cocaine exposure on full-term infant neurobehavioral functioning. Neurotoxicol Teratol 23:533–544.
57. Nieuwenhuys R (2012) The insular cortex: a review. Prog Brain Res 195: 123–163.
58. Noël X, Brevers D, Bechara A (2013) A neurocognitive approach to understanding the neurobiology of addiction. Curr Opin Neurobiol 23:632– 638.
59. Ohtani N, Goto T, Waeber C, Bhide PG (2003) Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci 23:2840–2850.
60. Paulus MP, Stewart JL (2014) Interoception and drug addiction. Neuropharmacology 76:342–350.
61. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154.
62. Rao H, Wang J, Giannetta J, Korczykowski M, Shera D, Avants BB, Gee J, Detre JA, Hurt H (2007) Altered resting cerebral blood flow in adolescents with in utero cocaine exposure revealed by perfusion functional MRI. Pediatrics 120:e1245–e1254.
63. Ren JQ, Malanga CJ, Tabit E, Kosofsky BE (2004) Neuropathological consequences of prenatal cocaine exposure in the mouse. Int J Dev Neurosci 22:309–320.
64. Roberts SC, Pies C (2011) Complex calculations: how drug use during pregnancy becomes a barrier to prenatal care. Matern Child Health J 15:333– 341.
65. Scher MS, Richardson GA, Day NL (2000) Effects of prenatal cocaine/crack and other drug exposure on electroencephalographic sleep studies at birth and one year. Pediatrics 105:39–48.
66. Sheinkopf SJ, Lester BM, Sanes JN, Eliassen JC, Hutchison ER, Seifer R, Lagasse LL, Durston S, Casey BJ (2009) Functional MRI and response inhibition in children exposed to cocaine in utero. Preliminary findings. Dev Neurosci 31:159–166.
67. Shen D, Davatzikos C (2004) Measuring temporal morphological changes robustly in brain MR images via 4-dimensional template warping. Neuroimage 21:1508–1517.
68. Shi F, Yap PT, Wu G, Jia H, Gilmore JH, Lin W, Shen D (2011) Infant brain atlases from neonates to 1- and 2-year-olds. PLoS One 6:e18746–e18746.
69. Smith LM, Chang L, Yonekura ML, Gilbride K, Kuo J, Poland RE, Walot I, Ernst T (2001) Brain proton magnetic resonance spectroscopy and imaging in children exposed to cocaine in utero. Pediatrics 107:227–231.
70. Smyser CD, Inder TE, Shimony JS, Hill JE, Degnan AJ, Snyder AZ, Neil JJ (2010) Longitudinal analysis of neural network development in preterm infants. Cereb Cortex 20:2852–2862.
71. Song ZM, Undie AS, Koh PO, Fang YY, Zhang L, Dracheva S, Sealfon SC, Lidow MS (2002) D1 dopamine receptor regulation of microtubuleassociated protein-2 phosphorylation in developing cerebral cortical neurons. J Neurosci 22:6092–6105.
72. Sowell ER, Charness ME, Riley EP (2014) Pregnancy: No safe level of alcohol. Nature 513:172.
73. Supekar K, Musen M, Menon V (2009) Development of large-scale functional brain networks in children. PLoS Biol 7:e1000157.
74. Thomason ME, Dassanayake MT, Shen S, Katkuri Y, Alexis M, Anderson AL, Yeo L, Mody S, Hernandez-Andrade E, Hassan SS, Studholme C, Jeong JW, Romero R (2013) Cross-hemispheric functional connectivity in the human fetal brain. Sci Transl Med 5:173ra124.
75. Townsend JD, Torrisi SJ, Lieberman MD, Sugar CA, Bookheimer SY, Altshuler LL (2013) Frontal-amygdala connectivity alterations during emotion downregulation in bipolar I disorder. Biol Psychiatry 73:127– 135.
76. Ulfig N, Setzer M, Bohl J (2003) Ontogeny of the human amygdala. Ann N Y Acad Sci 985:22–33.
77. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8:443–459.
78. Wager TD, Phan KL, Liberzon I, Taylor SF (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. Neuroimage 19:513–531.
79. Wu CS, Jew CP, Lu HC (2011) Lasting impacts of prenatal cannabis exposure and the role of endogenous cannabinoids in the developing brain. Future Neurol 6:459–480.
80. Yumoto C, Jacobson SW, Jacobson JL (2008) Fetal substance exposure and cumulative environmental risk in an African American cohort. Child Dev 79:1761–1776.