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Long-Range Reduced Predictive Information Transfers of Autistic Youths in EEG Sensor-Space During Face Processing

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Abstract

The majority of previous functional/effective connectivity studies conducted on the autistic patients converged to the underconnectivity theory of ASD: “long-range underconnectivity and sometimes short-rang overconnectivity”. However, to the best of our knowledge the total (linear and nonlinear) predictive information transfers (PITs) of autistic patients have not been investigated yet. Also, EEG data have rarely been used for exploring the information processing deficits in autistic subjects. This study is aimed at comparing the total (linear and nonlinear) PITs of autistic and typically developing healthy youths during human face processing by using EEG data. The ERPs of 12 autistic youths and 19 age-matched healthy control (HC) subjects were recorded while they were watching upright and inverted human face images. The PITs among EEG channels were quantified using two measures separately: transfer entropy with self-prediction optimality (TESPO), and modified transfer entropy with self-prediction optimality (MTESPO). Afterwards, the directed differential connectivity graphs (dDCGs) were constructed to characterize the significant changes in the estimated PITs of autistic subjects compared with HC ones. By using both TESPO and MTESPO, long-range reduction of PITs of ASD group during face processing was revealed (particularly from frontal channels to right temporal channels). Also, it seemed the orientation of face images (upright or upside down) did not modulate the binary pattern of PIT-based dDCGs, significantly. Moreover, compared with TESPO, the results of MTESPO were more compatible with the underconnectivity theory of ASD in the sense that MTESPO showed no long-range increase in PIT. It is also noteworthy that to the best of our knowledge it is the first time that a version of MTE is applied for patients (here ASD) and it is also its first use for EEG data analysis.

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Notes

  1. Pervasive Development Disorder, Not Otherwise Specified.

  2. Prefrontal Cortex.

  3. Anterior Cingulate Cortex.

  4. Inferior Parietal Lobules.

  5. Inferior Frontal Gyrus.

  6. Fusiform Gyrus.

  7. Superior Temporal Gyrus.

  8. http://hemera-technologies-inc.software.informer.com.

  9. TIM 1.2.0 software by Kalle Rutanen (http://www.cs.tut.fi/~timhome/tim-1.2.0).

  10. Available at (http://trentool.github.io/TRENTOOL3).

  11. Right Fusiform Gyrus.

  12. Left Fusiform Gyrus.

References

  • American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, DSM-IV, 4th edn. American Psychiatric Association, Washington

    Google Scholar 

  • Amini L, Jutten C, Achard S, David O, Kahane P, Vercueil L, Minotti L, Hossein-Zadeh GA, Soltanian-Zadeh H (2010a) Comparison of five directed graph measures for identification of leading interictal epileptic regions. Physiol Meas 31:1529–1546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Amini L, Jutten C, Achard S, David O, Soltanian-Zadeh H, Hossein-Zadeh GA, Kahne P, Minotti L, Vercueil L (2010b) Directed differential connectivity graph of interictal epileptiform discharges. IEEE Trans Biomed Eng 58(4):884–893

    Article  PubMed Central  PubMed  Google Scholar 

  • Ay N, Polani D (2008) Information flows in causal networks. Adv Complex Syst 11:17

    Article  Google Scholar 

  • Barttfeld P, Wicker B, Cukier S, Navarta S, Lew S, Sigman M (2011) A big-world network in ASD: dynamical connectivity analysis reflects a deficit in long-range connections and an excess of short-range connections. Neuropsychologia 49(2):254–263

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Bird G, Catmur C, Silani G, Frith C, Frith U (2006) Attention does not modulate neural responses to social stimuli in autism spectrum disorders. Neuroimage 31(4):1614–1624

    Article  PubMed  Google Scholar 

  • Cao LY (1997) Practical method for determining the minimum embedding dimension of a scalar time series. Physica D 110:43–50

    Article  Google Scholar 

  • Coben R, Mohammad-Rezazadeh I, Cannon R (2014) Using quantitative and analytic EEG methods in the understanding of connectivity in autism spectrum disorders: a theory of mixed over- and under-connectivity. Front Hum Neurosci 8:45

    Article  PubMed Central  PubMed  Google Scholar 

  • Courchesne E, Pierce K (2005) Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15(2):225–230

    Article  CAS  PubMed  Google Scholar 

  • Diaconescu AO, Jensen J, Wang H, Willeit M, Menon M, Kapur Sh, McIntosh AR (2011) Aberrant effective connectivity in schizophrenia patients during appetitive conditioning. Front Hum Neurosci. doi:10.3389/fnhum.2010.00239

    PubMed Central  PubMed  Google Scholar 

  • Faes L, Nollo G, Porta A (2013) Compensated transfer entropy as a tool for reliably estimating information transfer in physiological time series. Entropy 15:198–219

    Article  Google Scholar 

  • Fombonne E (2009) Epidemiology of pervasive developmental disorders. Pediatr Res 65(6):591–598

    Article  PubMed  Google Scholar 

  • Fu S, Chunliang F, Shichun G, Yuejia L, Raja P (2012) Neural adaptation provides evidence for categorical differences in processing of faces and Chinese characters: an ERP study of the N170. PLoS One 7(7):e41103

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878

    Article  PubMed  Google Scholar 

  • Gómez C, Lizier JT, Schaum M, Wollstadt P, Grützner C, Uhlhaas P, Freitag CM, Schlitt S, Bölte S, Hornero R, Wibral M (2014) Reduced predictable information in brain signals in autism spectrum disorder. Front Neuroinform 8:9

    Article  PubMed Central  PubMed  Google Scholar 

  • Gómez-Herrero G (2010) Brain connectivity analysis with EEG, Ph.D. Thesis, Department of Signal Processing, Tamper University of technology, Finland. Available online at http://www.germangh.com/papers.html

  • Gómez-Herrero G, Wu W, Rutanen K, Soriano MC, Pipa G, Vicente R (2015) Assessing coupling dynamics from an ensemble of time series. Entropy 17:1958–1970

    Article  Google Scholar 

  • Gourévitch B, Bouquin-Jeannès RL, Faucon G (2006) Linear and nonlinear causality between signals: methods, examples and neurophysiological applications. Biol Cybern 95:349–369

    Article  PubMed  Google Scholar 

  • Granger CWJ (1969) Investigating causal relations by econometric models and crossspectral methods. Econometrica 37:424–438

    Article  Google Scholar 

  • Hanson C, Hanson SJ, Ramsey J, Glymour C (2013) Atypical effective connectivity of social brain networks in individuals with autism. Brain Connect 3(6):578–589

    Article  PubMed  Google Scholar 

  • He B, Yang L, Wilke C, Yuan H (2011) Electrophysiological imaging of brain activity and connectivity—challenges and opportunities. IEEE Trans Biomed Eng 58(7):1918–1931

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes JR (2007) Autism: the first firm finding = underconnectivity? Epilepsy Behavior 11:20–24

    Article  PubMed  Google Scholar 

  • Ioannides AA, Mitsis GD (2010) Do we need to consider non-linear information flow in corticomuscular interaction? Clin Neurophysiol 121:272–273

    Article  PubMed  Google Scholar 

  • Just MA, Cherkassky VL, Keller TA, Minshew NJ (2004) Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127(8):1811–1821

    Article  PubMed  Google Scholar 

  • Khadem A, Hossein-Zadeh GA (2011) The role of instantaneous relations in the estimation of brain effective connectivity and a modified measure, ICBME 2011, pp. 238–243

  • Khorrami A, Tehrani-Doost M, Esteky H (2013) Comparison between Face and object processing in youths with autism spectrum disorder: an event related potentials study. Iranian J Psychiatry 8(4):179–187

    Google Scholar 

  • Kozachenko L, Leonenko N (1987) Sample estimate of the entropy of a random vector. Problemy Peredachi Informatsii 23:9

    Google Scholar 

  • Kraskov A, Stögbauer H, Grassberger P (2004) Estimating mutual information. Phys Rev E 69:066138

    Article  Google Scholar 

  • Lindner M, Vicente R, Priesemann V, Wibral M (2011) A Matlab open source toolbox to analyse information flow in time series data with transfer entropy. BMC Neurosci 12:119

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu Z, Zhang Y, Bai L, Yan H, Dai R, Zhong Ch, Wang H, Wei W, Xue T, Feng Y, You Y, Tian J (2012) Investigation of the effective connectivity of resting state networks in Alzheimer’s disease: a functional MRI study combining independent components analysis and multivariate Granger causality analysis. NMR Biomed 25(12):1311–1320

    Article  PubMed  Google Scholar 

  • Lizier JT, Prokopenko M, Zomaya AY (2010) Information modification and particle collisions in distributed computation. Chaos 20:037109

    Article  PubMed  Google Scholar 

  • Marinazzo D, Liao W, Chen H, Stramaglia S (2011) Nonlinear connectivity by Granger causality. Neuroimage 58(2):330–338

    Article  PubMed  Google Scholar 

  • Mash EJ, Barkley RA (2003) Child psychopathology. The Guilford Press, New York, pp 409–454

    Google Scholar 

  • Meng M, Cherian T, Singal G, Sinha P (2012) Lateralization of face processing in the human brain. Proc Biol Sci 279(1735):2052–2061

    Article  PubMed Central  PubMed  Google Scholar 

  • Myles BS, Bock SJ, Simpson RL (2001) Asperger syndrome diagnostic scale (ASDS). PRO-ED, Austin

    Google Scholar 

  • Newschaffer CJ, Croen LA, Daneils J et al (2007) The epidemiology of autism spectrum disorders. Annu Rev Public Health 28:235–258

    Article  PubMed  Google Scholar 

  • Ozonoff S, Goodlin-Jones BL, Solomon M (2005) Evidence-based assessment of autism spectrum disorders in children and adolescents. J Clin Child Adolesc Psychol 34:523–540

    Article  PubMed  Google Scholar 

  • Palau-Baduell M, Salvadó-Salvadó B, Clofent-Torrentó M, Valls-Santasusana A (2012) Autism and neural connectivity. Rev Neurol 54(1):S31–S39

    PubMed  Google Scholar 

  • Pereda E, Quiroga RQ, Bhattacharya J (2005) Nonlinear multivariate analysis of neurophysiological signals. Prog Neurobiol 77:1–37

    Article  PubMed  Google Scholar 

  • Pierce K, Muller RA, Ambrose J, Allen G, Courchesne E (2001) Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI. Brain 124:2059–2073

    Article  CAS  PubMed  Google Scholar 

  • Pollonini L, Patidar U, Situ N, Rezaie R, Papanicolaou AC, and Zouridakis G (2010) Functional connectivity networks in the autistic and healthy brain assessed using Granger causality. Conference proceedings of IEMBS 2010

  • Radulescu E, Minati L, Ganeshan B, Harrison NA, Gray MA, Beacher FD, Chatwin C, Young RC, Critchley HD (2013) Abnormalities in fronto-striatal connectivity within language networks relate to differences in grey-matter heterogeneity in Asperger syndrome. Neuroimage Clin 27(2):716–726

    Article  Google Scholar 

  • Ragwitz M, Kantz H (2002) Markov models from data by simple nonlinear time series predictors in delay embedding spaces. Phys Rev E 65:056201

    Article  Google Scholar 

  • Raven JC, Court JH, Raven J (1990) Raven’s coloured progressive matrices Oxford. Oxford Psychologists Press, Oxford

    Google Scholar 

  • Rippon G, Brock J, Brown C, Boucher J (2007) Disordered connectivity in the autistic brain: challenges for the ‘new psychophysiology’. Int J Psychophysiol 63:164–172

    Article  PubMed  Google Scholar 

  • Rossion B, Dricot L, Devolder A, Bodart JM, Crommelinck M, De Gelder B, Zoontjes R (2000) Hemispheric asymmetries for whole-based and part-based face processing in the human fusiform gyrus. J Cogn Neurosci 12(5):793–802

    Article  CAS  PubMed  Google Scholar 

  • Sato W, Toichi M, Uono Sh, Kochiyama T (2012) Impaired social brain network for processing dynamic facial expressions in autism spectrum disorders. BMC Neurosci 13:99

    Article  PubMed Central  PubMed  Google Scholar 

  • Schoffelen JM, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30:1857–1865

    Article  PubMed  Google Scholar 

  • Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85:461–464

    Article  CAS  PubMed  Google Scholar 

  • Shen MD, Shih P, Öttl B, Keehn B, Leyden KM, Gaffrey MS, Müller RA (2012) Atypical lexicosemantic function of extrastriate cortex in aurism spectrum disorder: evidence from functional and effective connectivity. Neuroimage 62(3):1780–1791

    Article  PubMed  Google Scholar 

  • Shih P, Shen MD, Öttl B, Keehn B, Gaffrey MS, Müller RA (2010) Atypical network connectivity for imitation in autism spectrum disorder. Neuropsychologia 48(10):2931–2939

    Article  PubMed Central  PubMed  Google Scholar 

  • Sporns O, Tononi G (2007) Structural determinants of functional brain dynamics. In: Jirsa VK, McIntosh AR (eds) Handbook of brain connectivity. Springer, Berlin, pp 117–119

    Chapter  Google Scholar 

  • Stam CJ (2005) Nonlinear dynamical analysis of EEG and MEG: review of an emerging field. Clin Neurophysiol 116:2266–2301

    Article  CAS  PubMed  Google Scholar 

  • Takens F (1981) Detecting strange attractors in turbulence. In: Rand DA, Young LS (eds) Dynamical systems and turbulence. Lecture notes in mathematics, vol 898. Springer, Berlin, pp 366–381

    Google Scholar 

  • Tsiaras V, Simos PG, Rezaie R, Sheth BR, Garyfallidis E, Castillo EM, Papanicolaou AC (2011) Extracting biomarkers of autism from MEG resting state functional connectivity networks. Comput Biol Med 41(12):1166–1177

    Article  PubMed  Google Scholar 

  • Vakorin VA, Krakovsk OA, McIntosh AR (2009) Confounding effects of indirect connections on causality estimation. J. Neurosci Meth 184:152–160

    Article  Google Scholar 

  • Vicente R, Wibral M, Lindner M, Pipa G (2011) Transfer entropy—a model-free measure of effective connectivity for the neurosciences. J Comput Neurosci 30(1):45–67

    Article  PubMed Central  PubMed  Google Scholar 

  • Vissers ME, Cohen MX, Geurts HM (2012) Brain connectivity and high functioning autism: a promising path of research that needs refined models, methodological convergence, and stronger behavioral links. Neurosci Biobehav Rev 36(1):604–625

    Article  PubMed  Google Scholar 

  • Wass S (2011) Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn 75(1):18–28

    Article  PubMed  Google Scholar 

  • Wibral M, Rahm B, Rieder M, Lindner M, Vicente R, Kaiser J (2011) Transfer entropy in magnetoencephalographic data: quantifying information flow in cortical and cerebellar networks. Prog Biophys Mol Biol 105:80–97

    Article  PubMed  Google Scholar 

  • Wibral M, Pampu N, Priesemann V, Siebenhühner F, Seiwert H, Lindner M, Lizier JT, Vicente R (2013) Measuring information-transfer delays. PLoS One 8(2):e55809

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wibral M, Lizier JT, Vögler S, Priesemann V, Galuske R (2014) Local active information storage as a tool to understand distributed neural information processing. Front Neuroinform 8:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Wibral M, Lizier JT, Priesemann V (2015) Bits from brains for biologically inspired computing. Front Robot AI 2:5

    Article  Google Scholar 

  • Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle Ch (2008) Abnormal cerebral effective connectivity during explicit emotional processing in adults with explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neur 3:135–143

    Article  Google Scholar 

  • Wiener N (1956) The theory of prediction. In: Beckenbach EF (ed) Modern mathematics for engineers, vol 1. McGraw-Hill, New York

    Google Scholar 

  • Wollstadt P, Martínez-Zarzuela M, Vicente R, Díaz-Pernas FJ, Wibral M (2014) Efficient transfer entropy analysis of non-stationary neural time series. PLoS One 9(7):e102833

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Prof. Hossein Esteky, from School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran for letting us use his laboratory for EEG data acquisition.

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Correspondence to Gholam-Ali Hossein-Zadeh.

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Khadem, A., Hossein-Zadeh, GA. & Khorrami, A. Long-Range Reduced Predictive Information Transfers of Autistic Youths in EEG Sensor-Space During Face Processing. Brain Topogr 29, 283–295 (2016). https://doi.org/10.1007/s10548-015-0452-4

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