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Neural networks related to dysfunctional face processing in autism spectrum disorder

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Abstract

One of the most consistent neuropsychological findings in autism spectrum disorders (ASD) is a reduced interest in and impaired processing of human faces. We conducted an activation likelihood estimation meta-analysis on 14 functional imaging studies on neural correlates of face processing enrolling a total of 164 ASD patients. Subsequently, normative whole-brain functional connectivity maps for the identified regions of significant convergence were computed for the task-independent (resting-state) and task-dependent (co-activations) state in healthy subjects. Quantitative functional decoding was performed by reference to the BrainMap database. Finally, we examined the overlap of the delineated network with the results of a previous meta-analysis on structural abnormalities in ASD as well as with brain regions involved in human action observation/imitation. We found a single cluster in the left fusiform gyrus showing significantly reduced activation during face processing in ASD across all studies. Both task-dependent and task-independent analyses indicated significant functional connectivity of this region with the temporo-occipital and lateral occipital cortex, the inferior frontal and parietal cortices, the thalamus and the amygdala. Quantitative reverse inference then indicated an association of these regions mainly with face processing, affective processing, and language-related tasks. Moreover, we found that the cortex in the region of right area V5 displaying structural changes in ASD patients showed consistent connectivity with the region showing aberrant responses in the context of face processing. Finally, this network was also implicated in the human action observation/imitation network. In summary, our findings thus suggest a functionally and structurally disturbed network of occipital regions related primarily to face (but potentially also language) processing, which interact with inferior frontal as well as limbic regions and may be the core of aberrant face processing and reduced interest in faces in ASD.

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References

  • Amft M, Bzdok D, Laird AR, Fox PT, Schilbach L, Eickhoff SB (2014) Definition and characterization of an extended social-affective default network. Brain Struct Funct (Epub ahead of print)

  • Amunts K, Kedo O, Kindler M, Pieperhoff P, Mohlberg H, Shah NJ, Habel U, Schneider F, Zilles K (2005) Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol (Berl) 210:343–352

    CAS  Google Scholar 

  • Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26:839–851

    PubMed  Google Scholar 

  • Ashwin C, Baron-Cohen S, Wheelwright S, O’Riordan M, Bullmore ET (2007) Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger syndrome. Neuropsychologia 45(1):2–14

    PubMed  Google Scholar 

  • Avidan G, Behrmann M (2009) Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia. Curr Biol 19(13):1146–1150

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, Williams SC (1999) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11:1891–1898

    CAS  PubMed  Google Scholar 

  • Baron-Cohen S, Ring HA, Bullmore ET, Wheelwright S, Ashwin C, Williams SC (2000) The amygdala theory of autism. Neurosci Biobehav Rev 24:355–364

    CAS  PubMed  Google Scholar 

  • Bertone A, Mottron L, Jelenic P, Faubert J (2003) Motion perception in autism: a “complex” issue. J Cogn Neurosci 15:218–225

    PubMed  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

    PubMed  Google Scholar 

  • Blake R, Turner LM, Smoski MJ, Pozdol SL, Stone WL (2003) Visual recognition of biological motion is impaired in children with autism. Psychol Sci 14:151–157

    PubMed  Google Scholar 

  • Bookheimer SY, Wang AT, Scott A, Sigman M, Dapretto M (2008) Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. J Int Neuropsychol Soc 14(6):922–932

    PubMed Central  PubMed  Google Scholar 

  • Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17:875–887

    CAS  PubMed  Google Scholar 

  • Bzdok D, Laird AR, Zilles K, Fox PT, Eickhoff SB (2013) An investigation of the structural, connectional, and functional subspecialization in the human amygdala. Hum Brain Mapp 34(12):3247–3266

    PubMed  Google Scholar 

  • Campbell R, Lawrence K, Mandy W, Mitra C, Jeyakuma L, Skuse D (2006) Meanings in motion and faces: developmental associations between the processing of intention from geometrical animations and gaze detection accuracy. Dev Psychopathol 18(1):99–118

    PubMed  Google Scholar 

  • Caron MJ, Mottron L, Rainville C, Chouinard S (2004) Do high functioning persons with autism present superior spatial abilities? Neuropsychologia 42:467–481

    PubMed  Google Scholar 

  • Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50(3):1148–1167

    PubMed  Google Scholar 

  • Caspers J, Zilles K, Amunts K, Laird AR, Fox PT, Eickhoff SB (2013) Functional characterization and connectivity of two cytoarchitectonic visual areas on the human posterior fusiform gyrus. Hum Brain Mapp. doi:10.1002/hbm.22364

    Google Scholar 

  • Catarino A, Luke L, Waldman S, Andrade A, Fletcher PC, Ring H (2011) An fMRI investigation of detection of semantic incongruities in autistic spectrum conditions. Eur J Neurosci 33:558–567

    PubMed  Google Scholar 

  • Chan AW, Downing PE (2011) Faces and eyes in human lateral prefrontal cortex. Front Hum Neurosci 5:51

    PubMed Central  PubMed  Google Scholar 

  • Chartrand TL, Bargh JA (1999) The chameleon effect: the perception-behavior link and social interaction. J Personal Soc Psychol 76(6):893–910

    CAS  Google Scholar 

  • Cieslik EC, Zilles K, Caspers S, Roski C, Kellermann TS, Jakobs O, Langner R, Laird AR, Fox PT, Eickhoff SB (2013) Is there “one” DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb Cortex 23(11):2677–2689

    PubMed Central  PubMed  Google Scholar 

  • Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, Rowe A, Phillips M, McAlonan G, Howlin P, Murphy DG (2000) The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 123:2203–2212

    PubMed  Google Scholar 

  • Çukur T, Huth AG, Nishimoto S, Gallant JL (2013) Functional subdomains within human FFA. J Neurosci 33(42):16748–16766

    PubMed Central  PubMed  Google Scholar 

  • Dakin S, Frith U (2005) Vagaries of visual perception in autism. Neuron 48:497–507

    CAS  PubMed  Google Scholar 

  • Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, Alexander AL, Davidson RJ (2005) Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 8(4):519–526

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, Iacoboni M (2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9(1):28–30

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6(1):13–34

    CAS  PubMed  Google Scholar 

  • Dawson G, Webb SJ, McPartland J (2005) Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol 27(3):403–424

    PubMed  Google Scholar 

  • Deeley Q, Daly EM, Surguladze S, Page L, Toal F, Robertson D, Curran S, Giampietro V, Seal M, Brammer MJ, Andrew C, Murphy K, Phillips ML, Murphy DG (2007) An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biol Psychiatry 62(3):207–217

    PubMed  Google Scholar 

  • Dichter GS (2012) Functional magnetic resonance imaging of autism spectrum disorders. Dialogues Clin Neurosci 14(3):319–351

    PubMed Central  PubMed  Google Scholar 

  • Dichter GS, Belger A (2007) Social stimuli interfere with cognitive control in autism. Neuroimage 35(3):1219–1230

    PubMed Central  PubMed  Google Scholar 

  • Domes G, Kumbier E, Herpertz-Dahlmann B, Herpertz SC (2008) Social cognition in autism. A survey of functional imaging studies. Nervenarzt 79(3):261–274

    CAS  PubMed  Google Scholar 

  • Dumoulin SO, Bittar RG, Kabani NJ, Baker CL Jr, Le Goualher G, Bruce Pike G, Evans AC (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10(5):454–463

    CAS  PubMed  Google Scholar 

  • Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335

    PubMed  Google Scholar 

  • Eickhoff SB, Heim S, Zilles K, Amunts K (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32:570–582

    PubMed  Google Scholar 

  • Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans AC, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36(3):511–521

    PubMed  Google Scholar 

  • Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926

    PubMed Central  PubMed  Google Scholar 

  • Eickhoff SB, Jbabdi S, Caspers S, Laird AR, Fox PT, Zilles K, Behrens TE (2010) Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J Neurosci 30(18):6409–6421

    CAS  PubMed  Google Scholar 

  • Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361

    PubMed Central  PubMed  Google Scholar 

  • Eigsti IM, Schuh J, Mencl E, Schultz RT, Paul R (2011) The neural underpinnings of prosody in autism. Child Neuropsychol 18(6):600–617

    PubMed Central  PubMed  Google Scholar 

  • Eyler LT, Pierce K, Courchesne E (2012) A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. Brain 135:949–960

    PubMed Central  PubMed  Google Scholar 

  • Ferrari PF, Visalberghi E, Paukner A, Fogassi L, Ruggiero A, Suomi SJ (2006) Neonatal imitation in rhesus macaques. PLoS Biol 4(9):e302

    PubMed Central  PubMed  Google Scholar 

  • Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119(Pt 2):593–609

    PubMed  Google Scholar 

  • Gepner B, Mestre D, Masson G, de Schonen S (1995) Postural effects of motion vision in young autistic children. NeuroReport 6:1211–1214

    CAS  PubMed  Google Scholar 

  • Gervais H, Belin P, Boddaert N, Leboyer M, Coez A, Sfaello I, Barthélémy C, Brunelle F, Samson Y, Zilbovicius M (2004) Abnormal cortical voice processing in autism. Nat Neurosci 7:801–802

    CAS  PubMed  Google Scholar 

  • Goebel R, Khorram-Sefat D, Muckli L, Hacker H, Singer W (1998) The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur J Neurosci 10(5):1563–1573

    CAS  PubMed  Google Scholar 

  • Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25

    CAS  PubMed  Google Scholar 

  • Gotts SJ, Saad ZS, Jo HJ, Wallace GL, Cox RW, Martin A (2013) The perils of global signal regression for group comparisons: a case study of autism spectrum disorders. Front Hum Neurosci 7:356

    PubMed Central  PubMed  Google Scholar 

  • Groen WB, Tesink C, Petersson KM, van Berkum J, van der Gaag RJ, Hagoort P, Buitelaar JK (2010) Semantic, factual, and social language comprehension in adolescents with autism: an FMRI study. Cereb Cortex 20:1937–1945

    CAS  PubMed  Google Scholar 

  • Grosbras MH, Beaton S, Eickhoff SB (2012) Brain regions involved in human movement perception: a quantitative voxel-based meta-analysis. Hum Brain Mapp 33(2):431–454

    PubMed  Google Scholar 

  • Gur RC, Sara R, Hagendoorn M, Marom O, Hughett P, Macy L, Turner T, Bajcsy R, Posner A, Gur RE (2002) A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J Neurosci Methods 115(2):137–143

    PubMed  Google Scholar 

  • Herrington JD, Taylor JM, Grupe DW, Curby KM, Schultz RT (2011) Bidirectional communication between amygdala and fusiform gyrus during facial recognition. Neuroimage 56(4):2348–2355

    PubMed Central  PubMed  Google Scholar 

  • Hoffstaedter F, Grefkes C, Caspers S, Roski C, Palomero-Gallagher N, Laird AR, Fox PT, Eickhoff SB (2013) The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum Brain Mapp. doi:10.1002/hbm.22363

    PubMed  Google Scholar 

  • Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC (1998) Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 22(2):324–333

    CAS  PubMed  Google Scholar 

  • Hubl D, Bölte S, Feineis-Matthews S, Lanfermann H, Federspiel A, Strik W, Poustka F, Dierks T (2003) Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology 61(9):1232–1237

    CAS  PubMed  Google Scholar 

  • Iacoboni M (2005) Failure to deactivate in autism: the co-constitution of self and other. Trends Cogn Sci 10(10):431–433

    Google Scholar 

  • Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7(12):942–951

    CAS  PubMed  Google Scholar 

  • Ishai A (2008) Let’s face it: it’s a cortical network. Neuroimage 40(2):415–419

    PubMed  Google Scholar 

  • Jakobs O, Langner R, Caspers S, Roski C, Cieslik EC, Zilles K, Laird AR, Fox PT, Eickhoff SB (2012) Across-study and within-subject functional connectivity of a right temporo-parietal junction subregion involved in stimulus-context integration. Neuroimage 60(4):2389–2398

    PubMed Central  PubMed  Google Scholar 

  • Jolliffe T, Baron-Cohen S (1997) Are people with autism and Asperger syndrome faster than normal on the Embedded Figures Test? J Child Psychol Psychiatry 38:527–534

    CAS  PubMed  Google Scholar 

  • Jones EG (1986) Connectivity of the primate sensory-motor cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 5. Sensory-motor areas and aspects of cortical connectivity. Plenum, New York/London, pp 113–83

  • Joseph RM, Tager-Flusberg H (1997) An investigation of attention and affect in children with autism and Down syndrome. J Autism Dev Disord 27(4):385–396

    CAS  PubMed  Google Scholar 

  • Kana RK, Wadsworth HM (2012) “The archeologist’s career ended in ruins”: hemispheric differences in pun comprehension in autism. Neuroimage 62:77–86

    PubMed  Google Scholar 

  • Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA (2006) Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain 129(Pt 9):2484–2893

    PubMed  Google Scholar 

  • Kansaku K, Hashimoto K, Muraki S, Miura K, Takahashi T, Kawano K (2001) Retinotopic hemodynamic activation of the human V5/MT area during optokinetic responses. NeuroReport 12(18):3891–3895

    CAS  PubMed  Google Scholar 

  • Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17(11):4302–4311

    CAS  PubMed  Google Scholar 

  • Kanwisher N, Stanley D, Harris A (1999) The fusiform face area is selective for faces not animals. NeuroReport 10(1):183–187

    CAS  PubMed  Google Scholar 

  • Kleinhans NM, Richards T, Johnson LC, Weaver KE, Greenson J, Dawson G, Aylward E (2008) fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage 54:697–704

    Google Scholar 

  • Knaus TA, Silver AM, Lindgren KA, Hadjikhani N, Tager-Flusberg H (2008) fMRI activation during a language task in adolescents with ASD. J Int Neuropsychol Soc 14:967–979

    PubMed Central  PubMed  Google Scholar 

  • Kolster H, Peeters R, Orban GA (2010) The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. J Neurosci 30(29):9801–9820

    CAS  PubMed  Google Scholar 

  • Koshino H, Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA (2008) fMRI investigation of working memory for faces in autism: visual coding and underconnectivity with frontal areas. Cereb Cortex 18(2):289–300

    PubMed  Google Scholar 

  • Lahaie A, Mottron L, Arguin M, Berthiaume C, Jemel B, Saumier D (2006) Face perception in high-functioning autistic adults: evidence for superior processing of face parts, not for a configural face-processing deficit. Neuropsychology 20:30–41

    CAS  PubMed  Google Scholar 

  • Laird AR, Fox PM, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Turkeltaub PE, Kochunov P, Fox PT (2005) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164

    PubMed  Google Scholar 

  • Laird AR, Eickhoff SB, Li K, Robin DA, Glahn DC, Fox PT (2009) Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J Neurosci 29(46):14496–14505

    CAS  PubMed Central  PubMed  Google Scholar 

  • Laird AR, Eickhoff SB, Fox PM, Uecker AM, Ray KL, Saenz JJ Jr, McKay DR, Bzdok D, Laird RW, Robinson JL, Turner JA, Turkeltaub PE, Lancaster JL, Fox PT (2011) The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data. BMC Res Notes 4:349

    PubMed Central  PubMed  Google Scholar 

  • Macko KA, Jarvis CD, Kennedy C, Miyaoka M, Shinohara M, Sololoff L, Mishkin M (1982) Mapping the primate visual system with [2-14C]deoxyglucose. Science 218(4570):394–397

    CAS  PubMed  Google Scholar 

  • Malikovic A, Amunts K, Schleicher A, Mohlberg H, Eickhoff SB, Wilms M, Palomero-Gallagher N, Armstrong E, Zilles K (2007) Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb Cortex 17:562–574

    PubMed  Google Scholar 

  • Martin A, Chao LL (2001) Semantic memory and the brain: structure and processes. Curr Opin Neurobiol 11(2):194–201

    CAS  PubMed  Google Scholar 

  • Meltzoff AN, Moore MK (1977) Imitation of facial and manual gestures by human neonates. Science 198(4312):75–78

    CAS  PubMed  Google Scholar 

  • Merigan WH, Byrne CE, Maunsell JH (1991) Does primate motion perception depend on the magnocellular pathway? J Neurosci 11(11):3422–3429

    CAS  PubMed  Google Scholar 

  • Milne E, Swettenham J, Hansen P, Campbell R, Jeffries H, Plaisted K (2002) High motion coherence thresholds in children with autism. J Child Psychol Psychiatry 43:255–263

    PubMed  Google Scholar 

  • Mishkin M, Ungerleider LG (1982) Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav Brain Res 6(1):57–77

    CAS  PubMed  Google Scholar 

  • Mizuno A, Liu Y, Williams DL, Keller TA, Minshew NJ, Just MA (2011) The neural basis of deictic shifting in linguistic perspective-taking in high-functioning autism. Brain 134:2422–2435

    PubMed Central  PubMed  Google Scholar 

  • Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ (1996) A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383:812–815

    CAS  PubMed  Google Scholar 

  • Mottron L, Belleville S, Ménard E (1999) Local bias in autistic subjects as evidenced by graphic tasks: perceptual hierarchization or working memory deficit? J Child Psychol Psychiatry 40:743–755

    CAS  PubMed  Google Scholar 

  • Müller RA, Behen ME, Rothermel RD, Chugani DC, Muzik O, Mangner TJ, Chugani HT (1999) Brain mapping of language and auditory perception in high-functioning autistic adults: a PET study. J Autism Dev Disord 29:19–31

    PubMed  Google Scholar 

  • Müller VI, Habel U, Derntl B, Schneider F, Zilles K, Turetsky BI, Eickhoff SB (2011) Incongruence effects in crossmodal emotional integration. Neuroimage 54(3):2257–2266

    PubMed  Google Scholar 

  • Müller VI, Cieslik EC, Laird AR, Fox PT, Eickhoff SB (2013) Dysregulated left inferior parietal activity in schizophrenia and depression: functional connectivity and characterization. Front Hum Neurosci 12(7):268. doi:10.3389/fnhum.2013.00268

    Google Scholar 

  • Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2004) Imitation in neonatal chimpanzees (Pan troglodytes). Dev Sci 7(4):437–442

    PubMed  Google Scholar 

  • Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653–660

    PubMed  Google Scholar 

  • Nickl-Jockschat T, Habel U, Michel TM, Manning J, Laird AR, Fox PT, Schneider F, Eickhoff SB (2012) Brain structure anomalies in autism spectrum disorder–a meta-analysis of VBM studies using anatomic likelihood estimation. Hum Brain Mapp 33(6):1470–1489

    PubMed  Google Scholar 

  • Osterling J, Dawson G (1994) Early recognition of children with autism: a study of first birthday home videotapes. J Autism Dev Disord 24(3):247–257

    CAS  PubMed  Google Scholar 

  • Osterling JA, Dawson G, Munson JA (2002) Early recognition of 1-year-old infants with autism spectrum disorder versus mental retardation. Dev Psychopathol 14(2):239–251

    PubMed  Google Scholar 

  • Ousdal OT, Jensen J, Server A, Hariri AR, Nakstad PH, Andreassen OA (2008) The human amygdala is involved in general behavioral relevance detection: evidence from an event-related functional magnetic resonance imaging Go-NoGo task. Neuroscience 156:450–455

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pellicano E, Gibson L, Maybery M, Durkin K, Badcock DR (2005) Abnormal global processing along the dorsal visual pathway in autism: a possible mechanism for weak visuospatial coherence? Neuropsychologia 43:1044–1053

    PubMed  Google Scholar 

  • Pelphrey KA, Morris JP, McCarthy G, Labar KS (2007) Perception of dynamic changes in facial affect and identity in autism. Soc Cogn Affect Neurosci 2(2):140–149

    PubMed Central  PubMed  Google Scholar 

  • Pierce K, Haist F, Sedaghat F, Courchesne E (2004) The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain 127(Pt 12):2703–2716

    PubMed  Google Scholar 

  • Plaisted K, Swettenham J, Rees L (1999) Children with autism show local precedence in a divided attention task and global precedence in a selective attention task. Child Psychol Psychiatry 40:733–742

    CAS  Google Scholar 

  • Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74(3):1192–1199

    CAS  PubMed  Google Scholar 

  • Rajimehr R, Young JC, Tootell RB (2009) An anterior temporal face patch in human cortex, predicted by macaque maps. Proc Natl Acad Sci USA 106(6):1995–2000

    CAS  PubMed Central  PubMed  Google Scholar 

  • Redcay E, Courchesne E (2008) Deviant functional magnetic resonance imaging patterns of brain activity to speech in 2–3-year-old children with autism spectrum disorder. Biol Psychiatry 64:589–598

    PubMed Central  PubMed  Google Scholar 

  • Reetz K, Dogan I, Rolfs A, Binkofski F, Schulz JB, Laird AR, Fox PT, Eickhoff SB (2012) Investigating function and connectivity of morphometric findings—exemplified on cerebellar atrophy in spinocerebellar ataxia 17 (SCA17). Neuroimage 62(3):1354–1366

    PubMed  Google Scholar 

  • Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192

    CAS  PubMed  Google Scholar 

  • Rottschy C, Kleiman A, Dogan I, Langner R, Mirzazade S, Kronenbuerger M, Werner C, Shah NJ, Schulz JB, Eickhoff SB, Reetz K (2013a) Diminished activation of motor working-memory networks in Parkinson’s disease. PLoS One 8(4):e61786. doi:10.1371/journal.pone.0061786

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rottschy C, Caspers S, Roski C, Reetz K, Dogan I, Schulz JB, Zilles K, Laird AR, Fox PT, Eickhoff SB (2013b) Differentiated parietal connectivity of frontal regions for “what” and “where” memory. Brain Struct Funct 218(6):1551–1567

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saad ZS, Gotts SJ, Murphy K, Chen G, Jo HJ, Martin A, Cox RW (2012) Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect 2(1):25–32

    PubMed Central  PubMed  Google Scholar 

  • Sabatinelli D, Fortune EE, Li Q, Siddiqui A, Krafft C, Oliver WT, Beck S, Jeffries J (2011) Emotional perception: meta-analyses of face and natural scene processing. Neuroimage 54(3):2524–2533

    PubMed  Google Scholar 

  • Sander D, Grafman J, Zalla T (2003) The human amygdala: an evolved system for relevance detection. Rev Neurosci 14:303–316

    PubMed  Google Scholar 

  • Satterthwaite TD, Elliott MA, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RC, Gur RE, Wolf DH (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240–256

    PubMed  Google Scholar 

  • Schneider F, Heimann H, Himer W, Huss D, Mattes R, Adam B (1990) Computer-based analysis of facial action in schizophrenic and depressed patients. Eur Arch Psychiatry Clin Neurosci 240(2):67–76

    CAS  PubMed  Google Scholar 

  • Schneider F, Gur RC, Koch K, Backes V, Amunts K, Shah NJ, Bilker W, Gur RE, Habel U (2006) Impairment in the specificity of emotion processing in schizophrenia. Am J Psychiatry 163(3):442–447

    PubMed  Google Scholar 

  • Schulte-Rüther M, Greimel E, Markowitsch HJ, Kamp-Becker I, Remschmidt H, Fink GR, Piefke M (2011) Dysfunctions in brain networks supporting empathy: an fMRI study in adults with autism spectrum disorders. Soc Neurosci 6(1):1–21

    PubMed Central  PubMed  Google Scholar 

  • Shah A, Frith U (1983) An islet of ability in autistic children: a research note. J Child Psychol Psychiatry 24:613–620

    CAS  PubMed  Google Scholar 

  • Shah A, Frith U (1993) Why do autistic individuals show superior performance on the block design task? J Child Psychol Psychiatry 34:1351–1364

    CAS  PubMed  Google Scholar 

  • Spencer J, O’Brien J, Riggs K, Braddick O, Atkinson J, Wattam-Bell J (2000) Motion processing in autism: evidence for a dorsal stream deficiency. NeuroReport 11:2765–2767

    CAS  PubMed  Google Scholar 

  • Tesink CM, Buitelaar JK, Petersson KM, van der Gaag RJ, Kan CC, Tendolkar I, Hagoort P (2009) Neural correlates of pragmatic language comprehension in autism spectrum disorders. Brain 132:1941–1952

    CAS  PubMed  Google Scholar 

  • Tomasello M, Carpenter M (2005) The emergence of social cognition in three young chimpanzees. Monogr Soc Res Child Dev 70(1):vii-132

  • Tootell RB, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Brady TJ, Rosen BR (1995) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375:139–141

    CAS  PubMed  Google Scholar 

  • Turk DJ, Rosenblum AC, Gazzaniga MS, Macrae CN (2005) Seeing John Malkovich: the neural substrates of person categorization. Neuroimage 24(4):1147–1153

    PubMed  Google Scholar 

  • Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 16:765–780

    PubMed  Google Scholar 

  • Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P (2012) Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Hum Brain Mapp 33(1):1–13

    PubMed  Google Scholar 

  • Ungerleider LG, Haxby JV (1994) ‘What and ‘where’ in the human brain. Curr Opin Neurobiol 4(2):157–165

    CAS  PubMed  Google Scholar 

  • van Kooten IA, Palmen SJ, von Cappeln P, Steinbusch HW, Korr H, Heinsen H, Hof PR, van Engeland H, Schmitz C (2008) Neurons in the fusiform gyrus are fewer and smaller in autism. Brain 131(Pt 4):987–999

    PubMed  Google Scholar 

  • Vogt S, Buccino G, Wohlschläger AM, Canessa N, Shah NJ, Zilles K, Eickhoff SB, Freund HJ, Rizzolatti G, Fink GR (2007) Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise. Neuroimage 37(4):1371–1383

    PubMed  Google Scholar 

  • Vuilleumier P, Armony JL, Driver J, Dolan RJ (2001) Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30:829–841

    CAS  PubMed  Google Scholar 

  • Wallace GL, Dankner N, Kenworthy L, Giedd JN, Martin A (2010) Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain 133(Pt 12):3745–3754

    PubMed Central  PubMed  Google Scholar 

  • Wang J, Zhou T, Qiu M, Du A, Cai K, Wang Z, Zhou C, Meng M, Zhuo Y, Fan S, Chen L (1999) Relationship between ventral stream for object vision and dorsal stream for spatial vision: an fMRI + ERP study. Hum Brain Mapp 8(4):170–181

    CAS  PubMed  Google Scholar 

  • Wang AT, Dapretto M, Hariri AR, Sigman M, Bookheimer SY (2004) Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. Am Acad Child Adolesc Psychiatry 43(4):481–490

    Google Scholar 

  • Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Shipp S, Zeki S (1993) Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb Cortex 3:79–94

    CAS  PubMed  Google Scholar 

  • Weiner KS, Grill-Spector K (2010) Sparsely-distributed organization of face and limb activations in human ventral temporal cortex. Neuroimage 52(4):1559–1573

    PubMed Central  PubMed  Google Scholar 

  • Weiner KS, Grill-Spector K (2013) Neural representations of faces and limbs neighbor in human high-level visual cortex: evidence for a new organization principle. Psychol Res 77(1):74–97

    PubMed Central  PubMed  Google Scholar 

  • Weiner KS, Golarai G, Caspers J, Chuapoco MR, Mohlberg H, Zilles K, Amunts K, Grill-Spector K (2014) The mid-fusiform sulcus: a landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex. Neuroimage 84:453–465

    PubMed Central  PubMed  Google Scholar 

  • Williams JH, Whiten A, Suddendorf T, Perrett DI (2001) Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25(4):287–295

    CAS  PubMed  Google Scholar 

  • Wilms M, Eickhoff SB, Specht K, Amunts K, Shah NJ, Malikovic A, Fink GR (2005) Human V5/MT+: comparison of functional and cytoarchitectonic data. Anat Embryol (Berl) 210:485–495

    Google Scholar 

  • Zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60(1):162–169

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Authors and Affiliations

  1. Department of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Pauwelsstrasse 30, 52074, Aachen, Germany

    Thomas Nickl-Jockschat, Claudia Rottschy, Johanna Thommes & Frank Schneider

  2. Juelich-Aachen Research Alliance Brain, Juelich/Aachen, Germany

    Thomas Nickl-Jockschat, Claudia Rottschy & Frank Schneider

  3. Department of Physics, Florida International University, Miami, USA

    Angela R. Laird

  4. Research Imaging Institute, University of Texas Health Sciences Center, San Antonio, USA

    Peter T. Fox

  5. Institute of Clinical Neuroscience and Medical Psychology, Heinrich Heine University, Düsseldorf, Germany

    Simon B. Eickhoff

  6. Department of Neuroscience and Medicine, INM-1, Research Center Jülich, Jülich, Germany

    Claudia Rottschy & Simon B. Eickhoff

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  1. Thomas Nickl-Jockschat
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  2. Claudia Rottschy
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  3. Johanna Thommes
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  4. Frank Schneider
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  5. Angela R. Laird
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  6. Peter T. Fox
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  7. Simon B. Eickhoff
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Correspondence to Thomas Nickl-Jockschat.

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Nickl-Jockschat, T., Rottschy, C., Thommes, J. et al. Neural networks related to dysfunctional face processing in autism spectrum disorder. Brain Struct Funct 220, 2355–2371 (2015). https://doi.org/10.1007/s00429-014-0791-z

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  • DOI: https://doi.org/10.1007/s00429-014-0791-z

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