Skip to main content
Top
Published in: Journal of Neurodevelopmental Disorders 1/2018

Open Access 01-12-2018 | Research

Arterial spin labeling provides a reliable neurobiological marker of autism spectrum disorder

Authors: Benjamin E. Yerys, John D. Herrington, Gregory K. Bartley, Hua-Shan Liu, John A. Detre, Robert T. Schultz

Published in: Journal of Neurodevelopmental Disorders | Issue 1/2018

Login to get access

Abstract

Background

Research on neurobiological markers of autism spectrum disorder (ASD) has been elusive. However, radionuclide studies of cerebral blood flow (CBF) have shown decreased blood flow (hypoperfusion) in the temporal lobes of individuals with ASD across ages and intelligence. This observation fits with current neuroscientific models that implicate temporal regions in social perception and social cognition. Arterial spin labeled perfusion MRI allows noninvasive quantification of regional CBF as part of a multimodal MRI protocol. This method is almost entirely absent from ASD research to date. Our a priori hypothesis was that children with ASD would present with hypoperfusion in the temporal lobes—most notably the fusiform gyrus (given its prominent role in ASD social perception deficits). We also sought to examine the reproducibility of CBF measures, and their relationship to individual differences in facial recognition and ASD symptoms.

Methods

A total of 58 males (33 with ASD) between the ages of 12 and 17 years participated in the study. All children completed two arterial spin labeling and structural (T1) scans using a 3 T Siemens Verio scanner approximately 8 weeks apart, as well as behavioral testing at time 1 that included diagnostic measures and the Benton Facial Recognition Test. CBF was the key dependent variable, as was facial recognition performance, and ASD symptoms. The two scans were used for reliability analyses.

Results

The ASD group showed hypoperfusion in the bilateral fusiform gyrus and in right inferior temporal gyrus. Intra-class correlations showed moderate to good reliability across time within both groups, and no diagnostic group × time interactions. CBF in the left fusiform gyrus was significantly positively correlated with facial recognition. No significant correlations were observed with core ASD symptoms.

Conclusions

Arterial spin labeling revealed hypoperfusion in children with ASD in regions critical to social perception and cognition. The left fusiform gyrus plays an important role in facial recognition, and greater CBF in this region was correlated with more normative facial recognition performance in children with ASD. This study takes an important first step in establishing CBF of the temporal lobes as a reliable marker of ASD.
Literature
1.
go back to reference Ohnishi T, Matsuda H, Hashimoto T, Kunihiro T, Nishikawa M, Uema T, et al. Abnormal regional cerebral blood flow in childhood autism. Brain. 2000;123(Pt 9):1838–44.CrossRef Ohnishi T, Matsuda H, Hashimoto T, Kunihiro T, Nishikawa M, Uema T, et al. Abnormal regional cerebral blood flow in childhood autism. Brain. 2000;123(Pt 9):1838–44.CrossRef
2.
go back to reference Zilbovicius M, Boddaert N, Belin P, Poline J-B, Remy P, Mangin J-F, et al. Temporal lobe dysfunction in childhood autism: a PET study. Am J Psychiatry. 2000;157:1988–93.CrossRef Zilbovicius M, Boddaert N, Belin P, Poline J-B, Remy P, Mangin J-F, et al. Temporal lobe dysfunction in childhood autism: a PET study. Am J Psychiatry. 2000;157:1988–93.CrossRef
3.
go back to reference Burroni L, Orsi A, Monti L, Hayek Y, Rocchi R, Vattimo AG. Regional cerebral blood flow in childhood autism: a Spet study with Spm evaluation. Nucl Med Commun. 2008;29:150–6.CrossRef Burroni L, Orsi A, Monti L, Hayek Y, Rocchi R, Vattimo AG. Regional cerebral blood flow in childhood autism: a Spet study with Spm evaluation. Nucl Med Commun. 2008;29:150–6.CrossRef
4.
go back to reference Gendry Meresse I, Zilbovicius M, Boddaert N, Robel L, Philippe A, Sfaello I, et al. Autism severity and temporal lobe functional abnormalities. Ann Neurol. 2005;58:466–9.CrossRef Gendry Meresse I, Zilbovicius M, Boddaert N, Robel L, Philippe A, Sfaello I, et al. Autism severity and temporal lobe functional abnormalities. Ann Neurol. 2005;58:466–9.CrossRef
5.
go back to reference Critchley HD, Daly EM, Bullmore ET, Williams SCR, Van Amelsvoort T, Robertson DM, et al. The functional neuroanatomy of social behaviourChanges in cerebral blood flow when people with autistic disorder process facial expressions. Brain. 2000;123:2203–12.CrossRef Critchley HD, Daly EM, Bullmore ET, Williams SCR, Van Amelsvoort T, Robertson DM, et al. The functional neuroanatomy of social behaviourChanges in cerebral blood flow when people with autistic disorder process facial expressions. Brain. 2000;123:2203–12.CrossRef
6.
go back to reference Starkstein SE, Vazquez S, Vrancic D, Nanclares V, Manes F, Piven J, et al. SPECT findings in mentally retarded autistic individuals. J Neuropsychiatry Clin Neurosci. 2000;12:370–5.CrossRef Starkstein SE, Vazquez S, Vrancic D, Nanclares V, Manes F, Piven J, et al. SPECT findings in mentally retarded autistic individuals. J Neuropsychiatry Clin Neurosci. 2000;12:370–5.CrossRef
7.
go back to reference George MSMD, Costa DCMD, Kouris K, Ring HAMRCP, Ell PJMD. Cerebral blood flow abnormalities in adults with infantile autism. J Nerv. 1992;180:413–7.CrossRef George MSMD, Costa DCMD, Kouris K, Ring HAMRCP, Ell PJMD. Cerebral blood flow abnormalities in adults with infantile autism. J Nerv. 1992;180:413–7.CrossRef
8.
go back to reference Yang WH, Jing J, Cheng MH, Wang X, Bao P, Wang QX. Regional cerebral blood flow in children with autism spectrum disorders: a quantitative 99mTc-ECD brain SPECT study with statistical parametric mapping evaluation. Chin Med J Engl. 2011;124:1362–6.PubMed Yang WH, Jing J, Cheng MH, Wang X, Bao P, Wang QX. Regional cerebral blood flow in children with autism spectrum disorders: a quantitative 99mTc-ECD brain SPECT study with statistical parametric mapping evaluation. Chin Med J Engl. 2011;124:1362–6.PubMed
9.
go back to reference Jann K, Hernandez LM, Beck-Pancer D, McCarron R, Smith RX, Dapretto M, et al. Altered resting perfusion and functional connectivity of default mode network in youth with autism spectrum disorder. Brain Behav. 2015;5.CrossRef Jann K, Hernandez LM, Beck-Pancer D, McCarron R, Smith RX, Dapretto M, et al. Altered resting perfusion and functional connectivity of default mode network in youth with autism spectrum disorder. Brain Behav. 2015;5.CrossRef
10.
go back to reference Lassen NA, Ingvar DH, Skinhøj E. Brain function and blood flow. Sci Am. 1978;239:62–71.CrossRef Lassen NA, Ingvar DH, Skinhøj E. Brain function and blood flow. Sci Am. 1978;239:62–71.CrossRef
11.
go back to reference Sokoloff L. Localization of functional activity in the central nervous system by measurement of glucose utilization with radioactive deoxyglucose. J Cereb Blood Flow Metab. 1981;1:7–36.CrossRef Sokoloff L. Localization of functional activity in the central nervous system by measurement of glucose utilization with radioactive deoxyglucose. J Cereb Blood Flow Metab. 1981;1:7–36.CrossRef
12.
go back to reference Tak S, Wang DJ, Polimeni JR, Yan L, Chen JJ. Dynamic and static contributions of the cerebrovasculature to the resting-state BOLD signal. NeuroImage. 2014;84:672–80.CrossRef Tak S, Wang DJ, Polimeni JR, Yan L, Chen JJ. Dynamic and static contributions of the cerebrovasculature to the resting-state BOLD signal. NeuroImage. 2014;84:672–80.CrossRef
13.
go back to reference Biswal BB, Kylen JV, Hyde JS. Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed. 1997;10:165–70.CrossRef Biswal BB, Kylen JV, Hyde JS. Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed. 1997;10:165–70.CrossRef
14.
go back to reference Chuang K-H, van Gelderen P, Merkle H, Bodurka J, Ikonomidou VN, Koretsky AP, et al. Mapping resting-state functional connectivity using perfusion MRI. NeuroImage. 2008;40:1595–605.CrossRef Chuang K-H, van Gelderen P, Merkle H, Bodurka J, Ikonomidou VN, Koretsky AP, et al. Mapping resting-state functional connectivity using perfusion MRI. NeuroImage. 2008;40:1595–605.CrossRef
15.
go back to reference Fukunaga M, Horovitz SG, de Zwart JA, van Gelderen P, Balkin TJ, Braun AR, et al. Metabolic origin of bold signal fluctuations in the absence of stimuli Journal of Cerebral Blood Flow &amp. Metabolism J Cereb Blood Flow Metab. 2008;28:1377–87.CrossRef Fukunaga M, Horovitz SG, de Zwart JA, van Gelderen P, Balkin TJ, Braun AR, et al. Metabolic origin of bold signal fluctuations in the absence of stimuli Journal of Cerebral Blood Flow &amp. Metabolism J Cereb Blood Flow Metab. 2008;28:1377–87.CrossRef
16.
go back to reference Liang X, Zou Q, He Y, Yang Y. Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proc Natl Acad Sci. 2013;110:1929–34.CrossRef Liang X, Zou Q, He Y, Yang Y. Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proc Natl Acad Sci. 2013;110:1929–34.CrossRef
17.
go back to reference Viviani R, Messina I, Walter M. Resting state functional connectivity in perfusion imaging: correlation maps with BOLD connectivity and resting state perfusion. PLoS One. 2011;6:e27050.CrossRef Viviani R, Messina I, Walter M. Resting state functional connectivity in perfusion imaging: correlation maps with BOLD connectivity and resting state perfusion. PLoS One. 2011;6:e27050.CrossRef
18.
go back to reference Zou Q, Wu CW, Stein EA, Zang Y, Yang Y. Static and dynamic characteristics of cerebral blood flow during the resting state. NeuroImage. 2009;48:515–24.CrossRef Zou Q, Wu CW, Stein EA, Zang Y, Yang Y. Static and dynamic characteristics of cerebral blood flow during the resting state. NeuroImage. 2009;48:515–24.CrossRef
19.
go back to reference Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci. 1992;89:212–6.CrossRef Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci. 1992;89:212–6.CrossRef
20.
go back to reference Chiron C, Raynaud C, Mazière B, Zilbovicius M, Laflamme L, Masure MC, et al. Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med Off Publ Soc Nucl Med. 1992;33:696–703. Chiron C, Raynaud C, Mazière B, Zilbovicius M, Laflamme L, Masure MC, et al. Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med Off Publ Soc Nucl Med. 1992;33:696–703.
21.
go back to reference Wang J, Licht DJ, Jahng G-H, Liu C-S, Rubin JT, Haselgrove J, et al. Pediatric perfusion imaging using pulsed arterial spin labeling. J Magn Reson Imaging JMRI. 2003;18:404–13.CrossRef Wang J, Licht DJ, Jahng G-H, Liu C-S, Rubin JT, Haselgrove J, et al. Pediatric perfusion imaging using pulsed arterial spin labeling. J Magn Reson Imaging JMRI. 2003;18:404–13.CrossRef
22.
go back to reference Wang J, Licht DJ. Pediatric perfusion MR imaging using arterial spin labeling. Neuroimaging Clin N Am. 2006;16:149–67 ix.CrossRef Wang J, Licht DJ. Pediatric perfusion MR imaging using arterial spin labeling. Neuroimaging Clin N Am. 2006;16:149–67 ix.CrossRef
23.
go back to reference Aguirre GK, Detre JA, Zarahn E, Alsop DC. Experimental design and the relative sensitivity of BOLD and perfusion fMRI. NeuroImage. 2002;15:488–500.CrossRef Aguirre GK, Detre JA, Zarahn E, Alsop DC. Experimental design and the relative sensitivity of BOLD and perfusion fMRI. NeuroImage. 2002;15:488–500.CrossRef
24.
go back to reference Wang J, Aguirre GK, Kimberg DY, Roc AC, Li L, Detre JA. Arterial spin labeling perfusion fMRI with very low task frequency. Magn Reson Med. 2003;49:796–802.CrossRef Wang J, Aguirre GK, Kimberg DY, Roc AC, Li L, Detre JA. Arterial spin labeling perfusion fMRI with very low task frequency. Magn Reson Med. 2003;49:796–802.CrossRef
25.
go back to reference Rao H, Wang J, Tang K, Pan W, Detre JA. Imaging brain activity during natural vision using CASL perfusion fMRI. Hum Brain Mapp. 2007;28:593–601.CrossRef Rao H, Wang J, Tang K, Pan W, Detre JA. Imaging brain activity during natural vision using CASL perfusion fMRI. Hum Brain Mapp. 2007;28:593–601.CrossRef
26.
go back to reference Xie L, Dolui S, Das SR, Stockbower GE, Daffner M, Rao H, et al. A brain stress test: cerebral perfusion during memory encoding in mild cognitive impairment. NeuroImage Clin. 2016;11:388–97.CrossRef Xie L, Dolui S, Das SR, Stockbower GE, Daffner M, Rao H, et al. A brain stress test: cerebral perfusion during memory encoding in mild cognitive impairment. NeuroImage Clin. 2016;11:388–97.CrossRef
27.
go back to reference Olson IR, Plotzker A, Ezzyat Y. The enigmatic temporal pole: a review of findings on social and emotional processing. Brain J Neurol. 2007;130:1718–31.CrossRef Olson IR, Plotzker A, Ezzyat Y. The enigmatic temporal pole: a review of findings on social and emotional processing. Brain J Neurol. 2007;130:1718–31.CrossRef
28.
go back to reference Pascual B, Masdeu JC, Hollenbeck M, Makris N, Insausti R, Ding S-L, et al. Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study. Cereb Cortex. 2015;25:680–702.CrossRef Pascual B, Masdeu JC, Hollenbeck M, Makris N, Insausti R, Ding S-L, et al. Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study. Cereb Cortex. 2015;25:680–702.CrossRef
29.
go back to reference Schultz RT. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci. 2005;23:125–41.CrossRef Schultz RT. Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. Int J Dev Neurosci. 2005;23:125–41.CrossRef
30.
go back to reference Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry. 2009;65:63–74.CrossRef Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry. 2009;65:63–74.CrossRef
31.
go back to reference Patriquin MA, DeRamus T, Libero LE, Laird A, Kana RK. Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder. Hum Brain Mapp. 2016;37:3957–78.CrossRef Patriquin MA, DeRamus T, Libero LE, Laird A, Kana RK. Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder. Hum Brain Mapp. 2016;37:3957–78.CrossRef
32.
go back to reference Nomi JS, Uddin LQ. Face processing in autism spectrum disorders: from brain regions to brain networks. Neuropsychologia. 2015;71:201–16.CrossRef Nomi JS, Uddin LQ. Face processing in autism spectrum disorders: from brain regions to brain networks. Neuropsychologia. 2015;71:201–16.CrossRef
33.
go back to reference Pelphrey KA, Shultz S, Hudac CM, Vander Wyk BC. Research review: constraining heterogeneity: the social brain and its development in autism spectrum disorder. J Child Psychol Psychiatry. 2011;52:631–44.CrossRef Pelphrey KA, Shultz S, Hudac CM, Vander Wyk BC. Research review: constraining heterogeneity: the social brain and its development in autism spectrum disorder. J Child Psychol Psychiatry. 2011;52:631–44.CrossRef
34.
go back to reference Dawson G, Webb SJ, McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005;27:403–24.CrossRef Dawson G, Webb SJ, McPartland J. Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Dev Neuropsychol. 2005;27:403–24.CrossRef
35.
go back to reference Harms MB, Martin A, Wallace GL. Facial emotion recognition in autism spectrum disorders: a review of behavioral and neuroimaging studies. Neuropsychol Rev. 2010;20:290–322.CrossRef Harms MB, Martin A, Wallace GL. Facial emotion recognition in autism spectrum disorders: a review of behavioral and neuroimaging studies. Neuropsychol Rev. 2010;20:290–322.CrossRef
36.
go back to reference van Rooij D, Anagnostou E, Arango C, Auzias G, Behrmann M, Busatto GF, et al. Cortical and Subcortical Brain Morphometry Differences Between Patients With Autism Spectrum Disorder and Healthy Individuals Across the Lifespan: Results From the ENIGMA ASD Working Group. Am J Psychiatry. 2017;175:359-69. van Rooij D, Anagnostou E, Arango C, Auzias G, Behrmann M, Busatto GF, et al. Cortical and Subcortical Brain Morphometry Differences Between Patients With Autism Spectrum Disorder and Healthy Individuals Across the Lifespan: Results From the ENIGMA ASD Working Group. Am J Psychiatry. 2017;175:359-69.
37.
go back to reference Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, et al. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry. 2000;57:331–40.CrossRef Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, et al. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry. 2000;57:331–40.CrossRef
38.
go back to reference American Psychiatric Association, DSM-5 Task Force. Diagnostic and statistical manual of mental disorders: DSM-5. Arlington: American Psychiatric Association; 2013.CrossRef American Psychiatric Association, DSM-5 Task Force. Diagnostic and statistical manual of mental disorders: DSM-5. Arlington: American Psychiatric Association; 2013.CrossRef
39.
go back to reference American Psychiatric Association. Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition. 4th ed. Arlington: American Psychiatric Publishing, Inc.; 2000. American Psychiatric Association. Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition. 4th ed. Arlington: American Psychiatric Publishing, Inc.; 2000.
40.
go back to reference Gotham K, Risi S, Pickles A, Lord C. The autism diagnostic observation schedule: revised algorithms for improved diagnostic validity. J Autism Dev Disord. 2007;37:613–27.CrossRef Gotham K, Risi S, Pickles A, Lord C. The autism diagnostic observation schedule: revised algorithms for improved diagnostic validity. J Autism Dev Disord. 2007;37:613–27.CrossRef
41.
go back to reference Lord C, Rutter M, Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24:659–85.CrossRef Lord C, Rutter M, Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24:659–85.CrossRef
42.
go back to reference Gadow KD, Sprafkin J. Child & Adolescent Symptom Inventory - fourth edition revised. Checkmate Plus: Stony Brook; 2010. Gadow KD, Sprafkin J. Child & Adolescent Symptom Inventory - fourth edition revised. Checkmate Plus: Stony Brook; 2010.
43.
go back to reference Elliott CD. Differential ability scales-II (DAS-II). Pearson Assessments: San Antonio; 2007. Elliott CD. Differential ability scales-II (DAS-II). Pearson Assessments: San Antonio; 2007.
44.
go back to reference Constantino JN, Gruber CP. Social responsiveness scale, second edition (SRS-2). Odessa: Psychological Assessment Resources; 2013. Constantino JN, Gruber CP. Social responsiveness scale, second edition (SRS-2). Odessa: Psychological Assessment Resources; 2013.
45.
go back to reference Sparrow SS, Cicchetti DV, Balla DA. Vineland adaptive behavior scales, second edition (Vineland-II). San Antonio: NCS Pearson; 2005. Sparrow SS, Cicchetti DV, Balla DA. Vineland adaptive behavior scales, second edition (Vineland-II). San Antonio: NCS Pearson; 2005.
46.
go back to reference Benton AL, Van Allen MW. Impairment in facial recognition in patients with cerebral disease. Cortex. 1968;4:344–58.CrossRef Benton AL, Van Allen MW. Impairment in facial recognition in patients with cerebral disease. Cortex. 1968;4:344–58.CrossRef
47.
go back to reference Jain V, Duda J, Avants B, Giannetta M, Xie SX, Roberts T, et al. Longitudinal reproducibility and accuracy of pseudo-continuous arterial spin-labeled perfusion MR imaging in typically developing children. Radiology. 2012;263:527–36.CrossRef Jain V, Duda J, Avants B, Giannetta M, Xie SX, Roberts T, et al. Longitudinal reproducibility and accuracy of pseudo-continuous arterial spin-labeled perfusion MR imaging in typically developing children. Radiology. 2012;263:527–36.CrossRef
48.
go back to reference Jenkinson M, Beckmann CF, TEJ B, Woolrich MW, Smith SM. FSL. NeuroImage. 2012;62:782–90.CrossRef Jenkinson M, Beckmann CF, TEJ B, Woolrich MW, Smith SM. FSL. NeuroImage. 2012;62:782–90.CrossRef
49.
go back to reference Wang Z, Aguirre GK, Rao H, Wang J, Fernández-Seara MA, Childress AR, et al. Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imaging. 2008;26:261–9.CrossRef Wang Z, Aguirre GK, Rao H, Wang J, Fernández-Seara MA, Childress AR, et al. Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. Magn Reson Imaging. 2008;26:261–9.CrossRef
50.
go back to reference Wang J, Alsop DC, Song HK, Maldjian JA, Tang K, Salvucci AE, et al. Arterial transit time imaging with flow encoding arterial spin tagging (FEAST). Magn Reson Med. 2003;50:599–607.CrossRef Wang J, Alsop DC, Song HK, Maldjian JA, Tang K, Salvucci AE, et al. Arterial transit time imaging with flow encoding arterial spin tagging (FEAST). Magn Reson Med. 2003;50:599–607.CrossRef
51.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17:825–41.CrossRef Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17:825–41.CrossRef
52.
go back to reference Woolrich M. Robust group analysis using outlier inference. NeuroImage. 2008;41:286–301.CrossRef Woolrich M. Robust group analysis using outlier inference. NeuroImage. 2008;41:286–301.CrossRef
53.
go back to reference Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, et al. Bayesian analysis of neuroimaging data in FSL. NeuroImage. 2009;45:S173–86.CrossRef Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, et al. Bayesian analysis of neuroimaging data in FSL. NeuroImage. 2009;45:S173–86.CrossRef
54.
go back to reference Hayasaka S, Nichols TE. Validating cluster size inference: random field and permutation methods. NeuroImage. 2003;20:2343–56.CrossRef Hayasaka S, Nichols TE. Validating cluster size inference: random field and permutation methods. NeuroImage. 2003;20:2343–56.CrossRef
55.
go back to reference Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15:1–25.CrossRef Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 2002;15:1–25.CrossRef
56.
go back to reference Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20:45–57.CrossRef Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging. 2001;20:45–57.CrossRef
59.
go back to reference Abbott AE, Nair A, Keown CL, Datko M, Jahedi A, Fishman I, et al. Patterns of atypical functional connectivity and behavioral links in autism differ between default, salience, and executive networks. Cereb Cortex. 2016;26:4034–45.CrossRef Abbott AE, Nair A, Keown CL, Datko M, Jahedi A, Fishman I, et al. Patterns of atypical functional connectivity and behavioral links in autism differ between default, salience, and executive networks. Cereb Cortex. 2016;26:4034–45.CrossRef
60.
go back to reference Grelotti DJ, Klin AJ, Gauthier I, Skudlarski P, Cohen DJ, Gore JC, et al. fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia. 2005;43:373–85.CrossRef Grelotti DJ, Klin AJ, Gauthier I, Skudlarski P, Cohen DJ, Gore JC, et al. fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia. 2005;43:373–85.CrossRef
61.
go back to reference Schultz RT, Grelotti DJ, Klin A, Kleinman J, Van der Gaag C, Marois R, et al. The role of the fusiform face area in social cognition: implications for the pathobiology of autism. Philos Trans R Soc Lond Ser B Biol Sci. 2003;358:415–27.CrossRef Schultz RT, Grelotti DJ, Klin A, Kleinman J, Van der Gaag C, Marois R, et al. The role of the fusiform face area in social cognition: implications for the pathobiology of autism. Philos Trans R Soc Lond Ser B Biol Sci. 2003;358:415–27.CrossRef
62.
go back to reference Kohls G, Yerys BE, Schultz RT. Striatal development in autism: repetitive behaviors and the reward circuitry. Biol Psychiatry. 2014;76:358–9.CrossRef Kohls G, Yerys BE, Schultz RT. Striatal development in autism: repetitive behaviors and the reward circuitry. Biol Psychiatry. 2014;76:358–9.CrossRef
63.
go back to reference Kohls G, Chevallier C, Troiani V, Schultz RT. Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications. J Neurodev Disord. 2012;4:10.CrossRef Kohls G, Chevallier C, Troiani V, Schultz RT. Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications. J Neurodev Disord. 2012;4:10.CrossRef
64.
go back to reference Hadjikhani N, Joseph RM, Snyder J, Chabris CF, Clark J, Steele S, et al. Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. NeuroImage. 2004;22:1141–50.CrossRef Hadjikhani N, Joseph RM, Snyder J, Chabris CF, Clark J, Steele S, et al. Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. NeuroImage. 2004;22:1141–50.CrossRef
65.
go back to reference Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H. Abnormal activation of the social brain during face perception in autism. Hum Brain Mapp. 2007;28:441–9.CrossRef Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H. Abnormal activation of the social brain during face perception in autism. Hum Brain Mapp. 2007;28:441–9.CrossRef
66.
go back to reference Bookheimer SY, Wang AT, Scott A, Sigman M, Dapretto M. Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. J Int Neuropsychol Soc. 2008;14:922–32.CrossRef Bookheimer SY, Wang AT, Scott A, Sigman M, Dapretto M. Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. J Int Neuropsychol Soc. 2008;14:922–32.CrossRef
67.
go back to reference Dalton KM, Nacewicz BM, Alexander AL, Davidson RJ. Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biol Psychiatry. 2007;61:512–20.CrossRef Dalton KM, Nacewicz BM, Alexander AL, Davidson RJ. Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biol Psychiatry. 2007;61:512–20.CrossRef
68.
go back to reference Pierce K, Müller RA, Ambrose J, Allen G, Courchesne E. Face processing occurs outside the fusiform “face area” in autism: evidence from functional MRI. Brain. 2001;124:2059–73.CrossRef Pierce K, Müller RA, Ambrose J, Allen G, Courchesne E. Face processing occurs outside the fusiform “face area” in autism: evidence from functional MRI. Brain. 2001;124:2059–73.CrossRef
69.
go back to reference Pierce K, Haist F, Sedaghat F, Courchesne E. The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain. 2004;127:2703–16.CrossRef Pierce K, Haist F, Sedaghat F, Courchesne E. The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. Brain. 2004;127:2703–16.CrossRef
70.
go back to reference Button KS, Ioannidis JPA, Mokrysz C, Nosek BA, Flint J, Robinson ESJ, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.CrossRef Button KS, Ioannidis JPA, Mokrysz C, Nosek BA, Flint J, Robinson ESJ, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.CrossRef
71.
go back to reference Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, et al. Brain Hyperconnectivity in children with autism and its links to social deficits. Cell Rep. 2013;5:738–47.CrossRef Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, et al. Brain Hyperconnectivity in children with autism and its links to social deficits. Cell Rep. 2013;5:738–47.CrossRef
Metadata
Title
Arterial spin labeling provides a reliable neurobiological marker of autism spectrum disorder
Authors
Benjamin E. Yerys
John D. Herrington
Gregory K. Bartley
Hua-Shan Liu
John A. Detre
Robert T. Schultz
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Neurodevelopmental Disorders / Issue 1/2018
Print ISSN: 1866-1947
Electronic ISSN: 1866-1955
DOI
https://doi.org/10.1186/s11689-018-9250-0

Other articles of this Issue 1/2018

Journal of Neurodevelopmental Disorders 1/2018 Go to the issue