Visual attention in preterm born adults: Specifically impaired attentional sub-mechanisms that link with altered intrinsic brain networks in a compensation-like mode

NeuroImage

Volumn 107, Issue , 2015, Pages 95-106

  Finke, Kathrin ^a,b   Neitzel, Julia ^a,c   Bäuml, Josef G ^c   Redel, Petra ^a   Müller, Hermann J ^a   Meng, Chun ^a,c   Jaekel, Julia ^d,f   Daamen, Marcel ^e   Scheef, Lukas ^e   Busch, Barbara ^e   Baumann, Nicole ^f   Boecker, Henning ^e   Bartmann, Peter ^e   Habekost, Thomas ^b   Wolke, Dieter ^f,g   Wohlschläger, Afra ^c   Sorg, Christian ^c  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e UNIVERSITY HOSPITAL BONN   (Germany)

^f UNIVERSITY OF WARWICK   (United Kingdom)

^g UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Compensation; Intrinsic brain networks; Preterm birth; Preterm born adults; Selective attention; Theory of visual attention

Indexed keywords

ADULT; ARTICLE; ATTENTION DISTURBANCE; COGNITION; CONNECTOME; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NERVE CELL NETWORK; OCCIPITAL CORTEX; PARIETAL CORTEX; PREMATURITY; PROSPECTIVE STUDY; RESTING STATE NETWORK; SELECTIVE ATTENTION; SHORT TERM MEMORY; VISUAL ATTENTION; VISUAL MEMORY; ATTENTION; DEPTH PERCEPTION; IMAGE PROCESSING; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; PSYCHOMOTOR PERFORMANCE; VISION;

ADULT; ATTENTION; COGNITION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; NERVE NET; PHOTIC STIMULATION; PRINCIPAL COMPONENT ANALYSIS; PSYCHOMOTOR PERFORMANCE; SPACE PERCEPTION; VISUAL PERCEPTION;

EID: 84917709116     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.11.062     Document Type: Article

References (98)

1. Allen E.A., Erhardt E.B., Damaraju E., Gruner W., Segall J.M., Silva R.F., et al. A baseline for the multivariate comparison of resting-state networks. Front. Syst. Neurosci. 2011, 5:2.
2. Anderson P., Doyle L.W. Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. J. Am. Med. Assoc. 2003, 289(24):3264-3272.
3. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26(3):839-851.
4. Atkinson J., Braddick O. Visual and visuocognitive development in children born very prematurely. Progress. Brain Res. 2007, 164:123-149.
5. Atkinson J., Braddick O. Visual attention in the first years: typical development and developmental disorders. Dev. Med. Child Neurol. 2012, 54(7):589-595.
6. Aylward G.P. Cognitive and neuropsychological outcomes: more than IQ scores. Ment. Retard. Dev. Disabil. Res. Rev. 2002, 8(4):234-240.
7. Ball G., Boardman J.P., Rueckert D., Aljabar P., Arichi T., Merchant N., et al. The effect of preterm birth on thalamic and cortical development. Cereb. Cortex 2012, 22(5):1016-1024.
8. Baron I.S., Rey-Casserly C. Extremely preterm birth outcome: a review of four decades of cognitive research. Neuropsychol. Rev. 2010, 20(4):430-452.
9. Bauer A. Ein Verfahren zur Messung des für das Bildungsverhalten relevanten Sozial Status (BRSS) - überarbeitete Fassng 1988, Deutsches Institut für Internationale Pädagogische Forschung, Frankfurt (Germany).
10. Bäuml J.G., Daamen M., Meng C., Neitzel J., Scheef L., Jaekel J., et al. Correspondence between aberrant intrinsic network connectivity and gray-matter volume in the ventral brain of preterm born adults. Cereb. Cortex 2014, (published ahead of print). 10.1093/cercor/bhu133.
11. Berkes P., Orban G., Lengyel M., Fiser J. Spontaneous cortical activity reveals hallmarks of an optimal internal model of the environment. Science 2011, 331(6013):83-87.
12. Bhutta A.T., Cleves M.A., Casey P.H., Cradock M.M., Anand K.J. Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. J. Am. Med. Assoc. 2002, 288(6):728-737.
13. Blencowe H., Cousens S., Oestergaard M.Z., Chou D., Moller A.B., Narwal R., et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 2012, 379(9832):2162-2172.
14. Bogon J., Finke K., Schulte-Körne G., Müller H.J., Schneider W.X., Stenneken P. Parameter-based assessment of disturbed and intact components of visual attention in children with developmental dyslexia. Dev. Sci. 2014, 17(5):697-713.
15. Bull R., Espy K.A., Wiebe S.A. Short-term memory, working memory, and executive functioning in preschoolers: longitudinal predictors of mathematical achievement at age 7years. Dev. Neuropsychol. 2008, 33(3):205-228.
16. Bundesen C. A theory of visual attention. Psychol. Rev. 1990, 97(4):523-547.
17. Bundesen C., Habekost T., Kyllingsbaek S. A neural theory of visual attention: bridging cognition and neurophysiology. Psychol. Rev. 2005, 112(2):291-328.
18. Caspersen I.D., Habekost T. Selective and sustained attention in children with spina bifida myelomeningocele. Child Neuropsychol. 2013, 19(1):55-77.
19. Constable R.T., Ment L.R., Vohr B.R., Kesler S.R., Fulbright R.K., Lacadie C., et al. Prematurely born children demonstrate white matter microstructural differences at 12years of age, relative to term control subjects: an investigation of group and gender effects. Pediatrics 2013, 121(2):306-316.
20. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3(3):201-215.
21. Cowan N. The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav. Brain Sci. 2001, 24(1):87-114.
22. Cowan N., Elliott J., Saults S., Morey C.C., Mattox S., Hismjatullina A., et al. On the capacity of attention: its estimation and role in working memory and cognitive aptitudes. Cogn. Psychol. 2005, 51:42-100.
23. Crick F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc. Natl. Acad. Sci. U. S. A. 1984, 81(14):4586-4590.
24. Damaraju E., Phillips J.R., Lowe J.R., Ohls R., Calhoun V.D., Caprihan A. Resting-state functional connectivity differences in premature children. Front. Syst. Neurosci. 2010, 4:23.
25. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., et al. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(37):13848-13853.
26. Damoiseaux J.S., Beckmann C.F., Arigita E.J., Barkhof F., Scheltens P., Stam C.J., et al. Reduced resting-state brain activity in the "default network" in normal aging. Cereb. Cortex 2008, 18(8):1856-1864.
27. D'Onofrio B.M., Class Q.A., Rickert M.E., Larsson H., Langstrom N., Lichtenstein P. Preterm birth and mortality and morbidity: a population-based quasi-experimental study. J. Am. Med. Assoc. 2013, 70(11):1231-1240.
28. Doria V., Beckmann C.F., Arichi T., Merchant N., Groppo M., Turkheimer F.E., et al. Emergence of resting state networks in the preterm human brain. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(46):20015-20020.
29. Dubowitz L.M., Dubowitz V., Goldberg C. Clinical assessment of gestational age in the newborn infant. J. Pediatr. 1970, 77(1):1-10.
30. Eikenes L., Lohaugen G.C., Brubakk A.M., Skranes J., Haberg A.K. Young adults born preterm with very low birth weight demonstrate widespread white matter alterations on brain DTI. NeuroImage 2011, 54(3):1774-1785.
31. Erhardt E.B., Rachakonda S., Bedrick E.J., Allen E.A., Adali T., Calhoun V.D. Comparison of multi-subject ICA methods for analysis of fMRI data. Hum. Brain Mapp. 2011, 32(12):2075-2095.
32. Finke K., Bublak P., Zihl J. Visual spatial and visual pattern working memory: neuropsychological evidence for a differential role of left and right dorsal visual brain. Neuropsychologia 2006, 44(4):649-661.
33. Finke K., Schwarzkopf W., Muller U., Frodl T., Muller H.J., Schneider W.X., et al. Disentangling the adult attention-deficit hyperactivity disorder endophenotype: parametric measurement of attention. J. Abnorm. Psychol. 2011, 120(4):890-901.
34. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8(9):700-711.
35. Fransson P., Skiold B., Horsch S., Nordell A., Blennow M., Lagercrantz H., et al. Resting-state networks in the infant brain. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(39):15531-15536.
36. Fransson P., Skiold B., Engstrom M., Hallberg B., Mosskin M., Aden U., et al. Spontaneous brain activity in the newborn brain during natural sleep-an fMRI study in infants born at full term. Pediatr. Res. 2009, 66(3):301-305.
37. Gathercole S.E., Pickering S.J. Working memory deficits in children with low achievements in the national curriculum at 7years of age. Br. J. Educ. Psychol. 2000, 70(2):177-194.
38. Gillebert C.R., Dyrholm M., Vangkilde S., Kyllingsbaek S., Peeters R., Vandenberghe R. Attentional priorities and access to short-term memory: parietal interactions. NeuroImage 2012, 62(3):1551-1562.
39. Gozzo Y., Vohr B., Lacadie C., Hampson M., Katz K.H., Maller-Kesselman J., et al. Alterations in neural connectivity in preterm children at school age. NeuroImage 2009, 48(2):458-463.
40. Habekost T., Rostrup E. Visual attention capacity after right hemisphere lesions. Neuropsychologia 2007, 45(7):1474-1488.
41. Habekost T., Starrfelt R. Visual attention capacity: a review of TVA-based patient studies. Scand. J. Psychol. 2009, 50(1):23-32.
42. Hack M., Taylor H.G. Perinatal brain injury in preterm infants and later neurobehavioral function. J. Am. Med. Assoc. 2000, 284(15):1973-1974.
43. Hack M., Flannery D.J., Schluchter M., Cartar L., Borawski E., Klein N. Outcomes in young adulthood for very-low-birth-weight infants. N. Engl. J. Med. 2002, 346(3):149-157.
44. Horovitz S.G., Fukunaga M., de Zwart J.A., van Gelderen P., Fulton S.C., Balkin T.J., et al. Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum. Brain Mapp. 2008, 29(6):671-682.
45. Jarvis H.L., Gathercole S.E. Verbal and non-verbal working memory and achievements on national curriculum tests at 11 and 14years of age. Educ. Child Psychol. 2003, 20(3):123-140.
46. Johnson S. Cognitive and behavioural outcomes following very preterm birth. Semin. Fetal Neonatal Med. 2007, 12(5):363-373.
47. Kanwisher N., Wojciulik E. Visual attention: insights from brain imaging. Nat. Rev. Neurosci. 2000, 1(2):91-100.
48. Kastner S., Ungerleider L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 2000, 23:315-341.
49. Kim D.J., Park B., Park H.J. Functional connectivity-based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI. Hum. Brain Mapp. 2013, 34(6):1371-1385.
50. Kiviniemi V., Starck T., Remes J., Long X., Nikkinen J., Haapea M., et al. Functional segmentation of the brain cortex using high model order group PICA. Hum. Brain Mapp. 2009, 30(12):3865-3886.
51. Kyllingsbæk S. Modelling visual attention. Behav. Res. Methods 2006, 38(1):123-133.
52. Laird A.R., Fox P.M., Eickhoff S.B., Turner J.A., Ray K.L., McKay D.R., et al. Behavioral interpretations of intrinsic connectivity networks. J. Cogn. Neurosci. 2011, 23(12):4022-4037.
53. Lewis C.M., Baldassarre A., Committeri G., Romani G.L., Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(41):17558-17563.
54. Luciana M., Lindeke L., Georgieff M., Mills M., Nelson C.A. Neurobehavioral evidence for working-memory deficits in school-aged children with histories of prematurity. Dev. Med. Child Neurol. 1999, 41(8):521-533.
55. Luck S.J., Vogel E.K. The capacity of visual working memory for features and conjunctions. Nature 1997, 390(6657):279-281.
56. Magen H., Emmanouil T.A., McMains S.A., Kastner S., Treisman A. Attentional demands predict short-term memory load response in posterior parietal cortex. Neuropsychologia 2009, 47(8-9):1790-1798.
57. McAlonan K., Cavanaugh J., Wurtz R.H. Guarding the gateway to cortex with attention in visual thalamus. Nature 2008, 456(7220):391-394.
58. McAvinue L.P., Habekost T., Johnson K.A., Kyllingsbaek S., Vangkilde S., Bundesen C., et al. Sustained attention, attentional selectivity, and attentional capacity across the lifespan. Atten. Percept. Psychophys. 2012, 74(8):1570-1582.
59. Meng C., Brandl F., Tahmasian M., Shao J., Manoliu A., Scherr M., et al. Aberrant topology of striatum's connectivity is associated with the number of episodes in depression. Brain 2013, 137(2):598-609.
60. Ment L.R., Hirtz D., Huppi P.S. Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol. 2009, 8(11):1042-1055.
61. Mulder H., Pitchford N.J., Hagger M.S., Marlow N. Development of executive function and attention in preterm children: a systematic review. Dev. Neuropsychol. 2009, 34(4):393-421.
62. Mullen K.M., Vohr B.R., Katz K.H., Schneider K.C., Lacadie C., Hampson M., et al. Preterm birth results in alterations in neural connectivity at age 16years. NeuroImage 2011, 54(4):2563-2570.
63. Murphy K., Bodurka J., Bandettini P.A. How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration. NeuroImage 2007, 34(2):565-574.
64. Myers E.H., Hampson M., Vohr B., Lacadie C., Frost S.J., Pugh K.R., et al. Functional connectivity to a right hemisphere language center in prematurely born adolescents. NeuroImage 2010, 51(4):1445-1452.
65. Nosarti C., Giouroukou E., Healy E., Rifkin L., Walshe M., Reichenberg A., et al. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain 2008, 131(1):205-217.
66. Olsen P., Myhrman A., Rantakallio P. Educational capacity of low birth weight children up to the age of 24. Early Hum. Dev. 1994, 36(3):191-203.
67. Padilla N., Alexandrou G., Blennow M., Lagercrantz H., Aden U. Brain growth gains and losses in extremely preterm infants at term. Cereb. Cortex 2014, (published ahead of print). 10.1093/cercor/bhu133.
68. Pavlova M.A., Krageloh-Mann I. Limitations on the developing preterm brain: impact of periventricular white matter lesions on brain connectivity and cognition. Brain 2013, 136(4):998-1011.
69. Peers P.V., Ludwig C.J., Rorden C., Cusack R., Bonfiglioli C., Bundesen C., et al. Attentional functions of parietal and frontal cortex. Cereb. Cortex 2005, 15(10):1469-1484.
70. Pierson C.R., Folkerth R.D., Billiards S.S., Trachtenberg F.L., Drinkwater M.E., Volpe J.J., et al. Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol. 2007, 114(6):619-631.
71. Prechtl H.F. Neurological sequelae of prenatal and perinatal complications. Br. Med. J. 1967, 4(5582):763-767.
72. Riedl V., Valet M., Woller A., Sorg C., Vogel D., Sprenger T., et al. Repeated pain induces adaptations of intrinsic brain activity to reflect past and predict future pain. NeuroImage 2011, 57(1):206-213.
73. Riegel K., Orth B., Wolke D., Osterlund K. Die Entwicklung gefährdet geborener Kinder bis zum 5 Lebensjahr 1995, Thieme, Stuttgart (Germany).
74. Saigal S., Doyle L.W. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008, 371(9608):261-269.
75. Salmaso N., Jablonska B., Scafidi J., Vaccarino F.M., Gallo V. Neurobiology of premature brain injury. Nat. Neurosci. 2014, 17(3):341-346.
76. Schafer R.J., Lacadie C., Vohr B., Kesler S.R., Katz K.H., Schneider K.C., et al. Alterations in functional connectivity for language in prematurely born adolescents. Brain 2009, 132(3):661-670.
77. Shum D., Neulinger K., O'Callaghan M., Mohay H. Attentional problems in children born very preterm or with extremely low birth weight at 7-9years. Arch. Clin. Neuropsychol. 2008, 23(1):103-112.
78. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., et al. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(31):13040-13045.
79. Smyser C.D., Inder T.E., Shimony J.S., Hill J.E., Degnan A.J., Snyder A.Z., et al. Longitudinal analysis of neural network development in preterm infants. Cereb. Cortex 2010, 20(12):2852-2862.
80. Sorg C., Myers N., Redel P., Bublak P., Riedl V., Manoliu A., et al. Asymmetric loss of parietal activity causes spatial bias in prodromal and mild Alzheimer's disease. Biol. Psychiatry 2012, 71(9):798-804.
81. Sperling G. The information available in brief visual presentations. Psychol. Monogr. 1960, 74(11):1.
82. Srinivasan L., Dutta R., Counsell S.J., Allsop J.M., Boardman J.P., Rutherford M.A., et al. Quantification of deep gray matter in preterm infants at term-equivalent age using manual volumetry of 3-Tesla magnetic resonance images. Pediatrics 2007, 119(4):759-765.
83. St Clair-Thompson H.L., Gathercole S.E. Executive functions and achievements in school: shifting, updating, inhibition, and working memory. Q. J. Exp. Physiol. 2006, 59(4):745-759.
84. Stenneken P., Egetemeir J., Schulte-Korne G., Muller H.J., Schneider W.X., Finke K. Slow perceptual processing at the core of developmental dyslexia: a parameter-based assessment of visual attention. Neuropsychologia 2011, 49(12):3454-3465.
85. Strang-Karlsson S., Andersson S., Paile-Hyvarinen M., Darby D., Hovi P., Raikkonen K., et al. Slower reaction times and impaired learning in young adults with birth weight <1500g. Pediatrics 2010, 125(1):e74-e82.
86. Taylor H.G., Minich N.M., Klein N., Hack M. Longitudinal outcomes of very low birth weight: neuropsychological findings. J. Int. Neuropsychol. Soc. 2004, 10(2):149-163.
87. Todd J.J., Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 2004, 428(6984):751-754.
88. van de Weijer-Bergsma E., Wijnroks L., Jongmans M.J. Attention development in infants and preschool children born preterm: a review. Infant Behav. Dev. 2008, 31(3):333-351.
89. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 2012, 59(1):431-438.
90. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., et al. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447(7140):83-86.
91. Volpe J.J. Neurologic outcome of prematurity. Arch. Neurol. 1998, 55(3):297-300.
92. Volpe J.J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009, 8(1):110-124.
93. Von Aster M., Neubauer A., Horn R. Wechsler Intelligenztest für Erwachsene (WIE). Deutschsprachige Bearbeitung und Adaptation des WAIS-III von David Wechsler 2006, Harcourt Test Services, Frankfurt am Main (Germany).
94. White T.P., Symington I., Castellanos N.P., Brittain P.J., Froudist Walsh S., Nam K.W., et al. Dysconnectivity of neurocognitive networks at rest in very-preterm born adults. NeuroImage 2014, 18(4):352-365.
95. Wiegand I., Tollner T., Habekost T., Dyrholm M., Muller H.J., Finke K. Distinct neural markers of TVA-based visual processing speed and short-term storage capacity parameters. Cereb. Cortex 2013, 24(8):1967-1978.
96. Wilke M., Hauser T.K., Krageloh-Mann I., Lidzba K. Specific impairment of functional connectivity between language regions in former early preterms. Hum. Brain Mapp. 2013, 35(7):3372-3384.
97. Wolke D., Meyer R. Cognitive status, language attainment, and prereading skills of 6-year-old very preterm children and their peers: the Bavarian Longitudinal Study. Dev. Med. Child Neurol. 1999, 41(2):94-109.
98. Xu Y., Chun M.M. Dissociable neural mechanisms supporting visual short-term memory for objects. Nature 2006, 440(7080):91-95.