TY - JOUR
T1 - Saccade dysmetria indicates attenuated visual exploration in autism spectrum disorder
AU - the EU-AIMS LEAP group
AU - Bast, Nico
AU - Mason, Luke
AU - Freitag, Christine M.
AU - Smith, Tim
AU - Portugal, Ana Maria
AU - Poustka, Luise
AU - Banaschewski, Tobias
AU - Johnson, Mark
AU - Ahmad, Jumana
AU - Ambrosino, Sara
AU - Auyeung, Bonnie
AU - Baron-Cohen, Simon
AU - Baumeister, Sarah
AU - Beckmann, Christian F.
AU - Bolte, Sven
AU - Bourgeron, Thomas
AU - Bours, Carsten
AU - Brammer, Michael
AU - Brandeis, Daniel
AU - Brogna, Claudia
AU - Bruijn, Yvette d.
AU - Buitelaar, Jan K.
AU - Chakrabarti, Bhismadev
AU - Charman, Tony
AU - Cornelissen, Ineke
AU - Crawley, Daisy
AU - Dell’Acqua, Flavio
AU - Dumas, Guillaume
AU - Durston, Sarah
AU - Ecker, Christine
AU - Faulkner, Jessica
AU - Frouin, Vincent
AU - Garces, Pilar
AU - Goyard, David
AU - Ham, Lindsay
AU - Hayward, Hannah
AU - Hipp, Joerg
AU - Holt, Rosemary
AU - Jones, Emily J.H.
AU - Kundu, Prantik
AU - Lai, Meng Chuan
AU - D’ardhuy, Xavier Liogier
AU - Lombardo, Michael V.
AU - Loth, Eva
AU - Lythgoe, David J.
AU - Mandl, Rene
AU - Marquand, Andre
AU - Mennes, Maarten
AU - Meyer-Lindenberg, Andreas
AU - Moessnang, Carolin
AU - Murphy, Declan G.M.
AU - Oakley, Bethany
AU - O’Dwyer, Laurence
AU - Oldehinkel, Marianne
AU - Oranje, Bob
AU - Pandina, Gahan
AU - Persico, Antonio M.
AU - Ruggeri, Barbara
AU - Ruigrok, Amber
AU - Sabet, Jessica
AU - Sacco, Roberto
AU - San Jose Caceres, Antonia
AU - Simonoff, Emily
AU - Spooren, Will
AU - Tillmann, Julian
AU - Toro, Roberto
AU - Tost, Heike
AU - Waldman, Jack
AU - Williams, Steve C.R.
AU - Wooldridge, Caroline
AU - Zwiers, Marcel P.
N1 - Funding Information:
This study was funded by EU AIMS and AIMS-2-TRIALS. EU-AIMS received support from the IMI Joint Undertaking (JU) under grant agreement no.115300, resources of which are composed of financial contribution from the European Union’s Seventh Framework Programme (FP7/2007-2013), from the European Federation of Pharmaceutical Industries and Associations (EFPIA) companies’ in kind contribution, and from Autism Speaks. AIMS-2-TRIALS received funding from the IMI 2 JU under grant agreement no. 777394. The JU receives support from the European Union’s Horizon 2020 research and innovation programme and EFPIA, Autism Speaks, Autistica, and the Simons Foundation Autism Research Initiative. The authors acknowledge the contributions of all members of the EU-AIMS LEAP group: Jumana Ahmad, Sara Ambrosino, Bonnie Auyeung, Simon Baron-Cohen, Sarah Baumeister, Christian F. Beckmann, Sven Bölte, Thomas Bourgeron, Carsten Bours, Michael Brammer, Daniel Brandeis, Claudia Brogna, Yvette de Bruijn, Jan K. Buitelaar, Bhismadev Chakrabarti, Tony Charman, Ineke Cornelissen, Daisy Crawley, Flavio Dell’Acqua, Guillaume Dumas, Sarah Durston, Christine Ecker, Jessica Faulkner, Vincent Frouin, Pilar Garcés, David Goyard, Lindsay Ham, Hannah Hayward, Joerg Hipp, Rosemary Holt, Emily J.H. Jones, Prantik Kundu, Meng-Chuan Lai, Xavier Liogier D’ardhuy, Michael V. Lombardo, Eva Loth, David J. Lythgoe, René Mandl, Andre Marquand, Maarten Mennes, Andreas Meyer-Lindenberg, Carolin Moessnang, Declan G.M. Murphy, Bethany Oakley, Laurence O’Dwyer, Marianne Oldehinkel, Bob Oranje, Gahan Pandina, Antonio M. Persico, Barbara Ruggeri, Amber Ruigrok, Jessica Sabet, Roberto Sacco, Antonia San José Cáceres, Emily Simonoff, Will Spooren, Julian Tillmann, Roberto Toro, Heike Tost, Jack Waldman, Steve C.R. Williams, Caroline Wooldridge, and Marcel P. Zwiers.
C.M.F. currently receives research funding by the German Ministry of Science and Education (BMBF), the German Research Association (DFG), and the European Commission. She receives royalties for books on ASD, ADHD, and MDD. She has served as consultant for Desitin and Roche in 2017. L.P. received conference support or speaker’s fee by Lilly, Shire, and Medice. T.B. served in an advisory or consultancy role for Lundbeck, Medice, Neurim Pharmaceuticals, Oberberg GmbH, and Shire. He received conference support or speaker’s fees by Lilly, Medice, Novartis, and Shire. He has been involved in clinical trials conducted by Shire and Viforpharma. He received royalties from Hogrefe, Kohlhammer, CIP Medien, and Oxford University Press. The present work is unrelated to the above grants and relationships. The remaining authors have declared that they have no competing or potential conflicts of interest.
PY - 2021/1/28
Y1 - 2021/1/28
N2 - Background: Visual exploration in autism spectrum disorder (ASD) is characterized by attenuated social attention. The underlying oculomotor function during visual exploration is understudied, whereas oculomotor function during restricted viewing suggested saccade dysmetria in ASD by altered pontocerebellar motor modulation. Methods: Oculomotor function was recorded using remote eye tracking in 142 ASD participants and 142 matched neurotypical controls during free viewing of naturalistic videos with and without human content. The sample was heterogenous concerning age (6–30 years), cognitive ability (60–140 IQ), and male/female ratio (3:1). Oculomotor function was defined as saccade, fixation, and pupil-dilation features that were compared between groups in linear mixed models. Oculomotor function was investigated as ASD classifier and features were correlated with clinical measures. Results: We observed decreased saccade duration (∆M = −0.50, CI [−0.21, −0.78]) and amplitude (∆M = −0.42, CI [−0.12, −0.72]), which was independent of human video content. We observed null findings concerning fixation and pupil-dilation features (POWER =.81). Oculomotor function is a valid ASD classifier comparable to social attention concerning discriminative power. Within ASD, saccade features correlated with measures of restricted and repetitive behavior. Conclusions: We conclude saccade dysmetria as ASD oculomotor phenotype relevant to visual exploration. Decreased saccade amplitude and duration indicate spatially clustered fixations that attenuate visual exploration and emphasize endogenous over exogenous attention. We propose altered pontocerebellar motor modulation as underlying mechanism that contributes to atypical (oculo-)motor coordination and attention function in ASD.
AB - Background: Visual exploration in autism spectrum disorder (ASD) is characterized by attenuated social attention. The underlying oculomotor function during visual exploration is understudied, whereas oculomotor function during restricted viewing suggested saccade dysmetria in ASD by altered pontocerebellar motor modulation. Methods: Oculomotor function was recorded using remote eye tracking in 142 ASD participants and 142 matched neurotypical controls during free viewing of naturalistic videos with and without human content. The sample was heterogenous concerning age (6–30 years), cognitive ability (60–140 IQ), and male/female ratio (3:1). Oculomotor function was defined as saccade, fixation, and pupil-dilation features that were compared between groups in linear mixed models. Oculomotor function was investigated as ASD classifier and features were correlated with clinical measures. Results: We observed decreased saccade duration (∆M = −0.50, CI [−0.21, −0.78]) and amplitude (∆M = −0.42, CI [−0.12, −0.72]), which was independent of human video content. We observed null findings concerning fixation and pupil-dilation features (POWER =.81). Oculomotor function is a valid ASD classifier comparable to social attention concerning discriminative power. Within ASD, saccade features correlated with measures of restricted and repetitive behavior. Conclusions: We conclude saccade dysmetria as ASD oculomotor phenotype relevant to visual exploration. Decreased saccade amplitude and duration indicate spatially clustered fixations that attenuate visual exploration and emphasize endogenous over exogenous attention. We propose altered pontocerebellar motor modulation as underlying mechanism that contributes to atypical (oculo-)motor coordination and attention function in ASD.
KW - biomarker
KW - brainstem
KW - cerebellum
KW - eye tracking
KW - locus coeruleus
KW - pupillometry
KW - visual attention
U2 - 10.1111/jcpp.13267
DO - 10.1111/jcpp.13267
M3 - Article
C2 - 32449956
AN - SCOPUS:85085525519
SN - 0021-9630
VL - 62
SP - 149
EP - 159
JO - Journal of Child Psychology and Psychiatry
JF - Journal of Child Psychology and Psychiatry
IS - 2
ER -