Journal of Neurodevelopmental Disorders | |
Abnormal late visual responses and alpha oscillations in neurofibromatosis type 1: a link to visual and attention deficits | |
Miguel Castelo-Branco1  Eduardo D Silva1  Jorge Saraiva2  Fabiana Ramos2  Otília C d’Almeida1  Maria J Ribeiro1  | |
[1] Visual Neuroscience Laboratory, Institute for Biomedical Imaging and Life Sciences (IBILI), Faculty of Medicine, University of Coimbra, Azinhaga de Santa Comba, Coimbra 3000-548, Portugal;Medical Genetics Department, Pediatric Hospital of Coimbra, Coimbra, Portugal | |
关键词: Paediatric; Neurofibromatosis type 1 (NF1); Electroencephalogram (EEG); Contrast response function; Alpha rhythm; Visual evoked potentials; | |
Others : 804532 DOI : 10.1186/1866-1955-6-4 |
|
received in 2013-09-12, accepted in 2014-01-24, 发布年份 2014 | |
【 摘 要 】
Background
Neurofibromatosis type 1 (NF1) affects several areas of cognitive function including visual processing and attention. We investigated the neural mechanisms underlying the visual deficits of children and adolescents with NF1 by studying visual evoked potentials (VEPs) and brain oscillations during visual stimulation and rest periods.
Methods
Electroencephalogram/event-related potential (EEG/ERP) responses were measured during visual processing (NF1 n = 17; controls n = 19) and idle periods with eyes closed and eyes open (NF1 n = 12; controls n = 14). Visual stimulation was chosen to bias activation of the three detection mechanisms: achromatic, red-green and blue-yellow.
Results
We found significant differences between the groups for late chromatic VEPs and a specific enhancement in the amplitude of the parieto-occipital alpha amplitude both during visual stimulation and idle periods. Alpha modulation and the negative influence of alpha oscillations in visual performance were found in both groups.
Conclusions
Our findings suggest abnormal later stages of visual processing and enhanced amplitude of alpha oscillations supporting the existence of deficits in basic sensory processing in NF1. Given the link between alpha oscillations, visual perception and attention, these results indicate a neural mechanism that might underlie the visual sensitivity deficits and increased lapses of attention observed in individuals with NF1.
【 授权许可】
2014 Ribeiro et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140708062836874.pdf | 1480KB | download | |
Figure 9. | 47KB | Image | download |
Figure 8. | 30KB | Image | download |
Figure 7. | 69KB | Image | download |
Figure 6. | 73KB | Image | download |
Figure 5. | 68KB | Image | download |
Figure 4. | 81KB | Image | download |
Figure 3. | 85KB | Image | download |
Figure 2. | 136KB | Image | download |
Figure 1. | 75KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.
【 参考文献 】
- [1]Levine TM, Materek A, Abel J, O’Donnell M, Cutting LE: Cognitive profile of neurofibromatosis type 1. Semin Pediatr Neurol 2006, 13:8-20.
- [2]Payne JM, Moharir MD, Webster R, North KN: Brain structure and function in neurofibromatosis type 1: current concepts and future directions. J Neurol Neurosurg Psychiatry 2010, 81:304-309.
- [3]Duarte JV, Ribeiro MJ, Violante IR, Cunha G, Silva E, Castelo-Branco M: Multivariate pattern analysis reveals subtle brain anomalies relevant to the cognitive phenotype in neurofibromatosis type 1. Hum Brain Mapp 2014, 35:89-106.
- [4]Violante IR, Ribeiro MJ, Edden RA, Guimaraes P, Bernardino I, Rebola J, Cunha G, Silva E, Castelo-Branco M: GABA deficit in the visual cortex of patients with neurofibromatosis type 1: genotype-phenotype correlations and functional impact. Brain 2013, 136:918-925.
- [5]Violante IR, Ribeiro MJ, Silva ED, Castelo-Branco M: Gyrification, cortical and subcortical morphometry in neurofibromatosis type 1: an uneven profile of developmental abnormalities. J Neurodev Disord 2013, 5:3.
- [6]Clements-Stephens AM, Rimrodt SL, Gaur P, Cutting LE: Visuospatial processing in children with neurofibromatosis type 1. Neuropsychologia 2008, 46:690-697.
- [7]Violante IR, Ribeiro MJ, Cunha G, Bernardino I, Duarte JV, Ramos F, Saraiva J, Silva E, Castelo-Branco M: Abnormal brain activation in neurofibromatosis type 1: a link between visual processing and the default mode network. PLoS One 2012, 7:e38785.
- [8]Ribeiro MJ, Violante IR, Bernardino I, Ramos F, Saraiva J, Reviriego P, Upadhyaya M, Silva ED, Castelo-Branco M: Abnormal achromatic and chromatic contrast sensitivity in Neurofibromatosis type 1. Invest Ophthalmol Vis Sci 2012, 53:287-293.
- [9]Cole GR, Hine T, McIlhagga W: Detection mechanisms in L-, M-, and S-cone contrast space. J Opt Soc Am A 1993, 10:38-51.
- [10]Merigan WH, Maunsell JH: How parallel are the primate visual pathways? Annu Rev Neurosci 1993, 16:369-402.
- [11]Callaway EM: Structure and function of parallel pathways in the primate early visual system. J Physiol 2005, 566:13-19.
- [12]Hendry SH, Reid RC: The koniocellular pathway in primate vision. Annu Rev Neurosci 2000, 23:127-153.
- [13]Mullen KT, Dumoulin SO, McMahon KL, de Zubicaray GI, Hess RF: Selectivity of human retinotopic visual cortex to S-cone-opponent, L/M-cone-opponent and achromatic stimulation. Eur J Neurosci 2007, 25:491-502.
- [14]Wandell BA, Poirson AB, Newsome WT, Baseler HA, Boynton GM, Huk A, Gandhi S, Sharpe LT: Color signals in human motion-selective cortex. Neuron 1999, 24:901-909.
- [15]Porciatti V, Bonanni P, Fiorentini A, Guerrini R: Lack of cortical contrast gain control in human photosensitive epilepsy. Nat Neurosci 2000, 3:259-263.
- [16]Krauskopf J, Williams DR, Heeley DW: Cardinal directions of color space. Vision Res 1982, 22:1123-1131.
- [17]Kulikowski JJ, Tolhurst DJ: Psychophysical evidence for sustained and transient detectors in human vision. J Physiol 1973, 232:149-162.
- [18]Jensen O, Mazaheri A: Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 2010, 4:186.
- [19]Mazaheri A, Coffey-Corina S, Mangun GR, Bekker EM, Berry AS, Corbett BA: Functional disconnection of frontal cortex and visual cortex in attention-deficit/hyperactivity disorder. Biol Psychiatry 2010, 67:617-623.
- [20]Uhlhaas PJ, Singer W: Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010, 11:100-113.
- [21]Rippon G, Brock J, Brown C, Boucher J: Disordered connectivity in the autistic brain: challenges for the "new psychophysiology". Int J Psychophysiol 2007, 63:164-172.
- [22]National Institutes of Health Consensus Development Conference: Neurofibromatosis Conference statement. National Institutes of Health Consensus Development Conference. Arch Neurol 1988, 45:575-578.
- [23]Ribeiro MJ, Castelo-Branco M: Psychophysical channels and ERP population responses in human visual cortex: Area summation across chromatic and achromatic pathways. Vision Res 2010, 50:1283-1291.
- [24]Cole GR, Hine T: Computations of cone contrasts for color vision research. Behaviour Research Methods Instruments and Computers 1992, 24:22-27.
- [25]Derrington AM, Krauskopf J, Lennie P: Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol 1984, 357:241-265.
- [26]MacLeod DI, Boynton RM: Chromaticity diagram showing cone excitation by stimuli of equal luminance. J Opt Soc Am 1979, 69:1183-1186.
- [27]Regan D: Some early uses of evoked brain responses in investigations of human visual function. Vision Res 2009, 49:882-897.
- [28]Luck SJ: An Introduction to the Event-Related Potential Technique. Cambridge, MA: MIT Press; 2005.
- [29]Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W: Neural synchrony and the development of cortical networks. Trends Cogn Sci 2010, 14:72-80.
- [30]Engell AD, McCarthy G: Selective attention modulates face-specific induced gamma oscillations recorded from ventral occipitotemporal cortex. J Neurosci 2010, 30:8780-8786.
- [31]Cottaris NP, De Valois RL: Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 1998, 395:896-900.
- [32]Payne JM, Hyman SL, Shores EA, North KN: Assessment of executive function and attention in children with neurofibromatosis type 1: relationships between cognitive measures and real-world behavior. Child Neuropsychol 2011, 17:313-329.
- [33]Niedermeyer E, da Silva FH L: The normal EEG of the waking adult. In Electroencephalography: Basic Principles, Clinical Applications and Related Fields. Edited by Niedermeyer E, da Silva FH L. Baltimore, MD: Lippincott Williams & Wilkins; 1999:149-173.
- [34]Klimesch W: EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 1999, 29:169-195.
- [35]Lidzba K, Granstrom S, Lindenau J, Mautner VF: The adverse influence of attention-deficit disorder with or without hyperactivity on cognition in neurofibromatosis type 1. Dev Med Child Neurol 2012, 54:892-897.
- [36]Hagler DJ Jr, Halgren E, Martinez A, Huang M, Hillyard SA, Dale AM: Source estimates for MEG/EEG visual evoked responses constrained by multiple, retinotopically-mapped stimulus locations. Hum Brain Mapp 2009, 30:1290-1309.
- [37]Petrov Y, Nador J, Qian J: VEP correlates of feedback in human cortex. PLoS One 2012, 7:e51791.
- [38]Di Russo F, Pitzalis S, Spitoni G, Aprile T, Patria F, Spinelli D, Hillyard SA: Identification of the neural sources of the pattern-reversal VEP. Neuroimage 2005, 24:874-886.
- [39]Gebber GL, Zhong S, Lewis C, Barman SM: Human brain alpha rhythm: nonlinear oscillation or filtered noise? Brain Res 1999, 818:556-560.
- [40]de Sa AMM, Infantosi AF: Evaluating the entrainment of the alpha rhythm during stroboscopic flash stimulation by means of coherence analysis. Med Eng Phys 2005, 27:167-173.
- [41]Herrmann CS: Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp Brain Res 2001, 137:346-353.
- [42]de Graaf TA, Gross J, Paterson G, Rusch T, Sack AT, Thut G: Alpha-band rhythms in visual task performance: phase-locking by rhythmic sensory stimulation. PLoS One 2013, 8:e60035.
- [43]Mathewson KE, Prudhomme C, Fabiani M, Beck DM, Lleras A, Gratton G: Making waves in the stream of consciousness: entraining oscillations in EEG alpha and fluctuations in visual awareness with rhythmic visual stimulation. J Cogn Neurosci 2012, 24:2321-2333.
- [44]van Dijk H, Schoffelen JM, Oostenveld R, Jensen O: Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 2008, 28:1816-1823.
- [45]Thut G, Nietzel A, Brandt SA, Pascual-Leone A: Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J Neurosci 2006, 26:9494-9502.
- [46]Romei V, Brodbeck V, Michel C, Amedi A, Pascual-Leone A, Thut G: Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex 2008, 18:2010-2018.
- [47]Romei V, Gross J, Thut G: On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J Neurosci 2010, 30:8692-8697.
- [48]Hoogenboom N, Schoffelen JM, Oostenveld R, Parkes LM, Fries P: Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 2006, 29:764-773.
- [49]Barry RJ, Clarke AR, Johnstone SJ, Brown CR: EEG differences in children between eyes-closed and eyes-open resting conditions. Clin Neurophysiol 2009, 120:1806-1811.
- [50]Foxe JJ, Snyder AC: The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention. Front Psychol 2011, 2:154.
- [51]Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M: Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci USA 2007, 104:13170-13175.
- [52]Weissman DH, Roberts KC, Visscher KM, Woldorff MG: The neural bases of momentary lapses in attention. Nat Neurosci 2006, 9:971-978.
- [53]Hughes SW, Crunelli V: Just a phase they’re going through: the complex interaction of intrinsic high-threshold bursting and gap junctions in the generation of thalamic alpha and theta rhythms. Int J Psychophysiol 2007, 64:3-17.