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Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation

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Antagonistic Interactions Between Microsaccades and Evidence Accumulation Processes During Decision Formation This Accepted Manuscript has not been copyedited and formatted. The final version may differ from this version. Research Articles: Behavioral/Cognitive Antagonistic interactions between microsaccades and evidence accumulation processes during decision formation Gerard M. Loughnane1, Daniel P. Newman2, Sarita Tamang3, Simon P. Kelly3,4 and Redmond G. O'Connell1 1Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin 2, Ireland. 2School of Psychological Sciences and Monash Institute for Cognitive and Clinical Neurosciences (MICCN), Monash University, Melbourne, VIC 3806, Australia. 3Department of Biomedical Engineering, City College of the City University of New York. 4School of Electrical and Electronic Engineering, University College Dublin, Dublin 4, Ireland. DOI: 10.1523/JNEUROSCI.2340-17.2018 Received: 18 August 2017 Revised: 20 December 2017 Accepted: 14 January 2018 Published: 25 January 2018 Author contributions: G.M.L., S.T., and S.P.K. designed research; G.M.L. and S.T. performed research; G.M.L., D.P.N., S.P.K., and R.G.O. analyzed data; G.M.L., D.P.N., S.P.K., and R.G.O. wrote the paper. Conflict of Interest: The authors declare no competing financial interests. This study was supported by grants from the United States National Science Foundation (BCS-1358955 to S.P.K. and R.G.O.), European Research Council (63829 to R.G.O.), and the International Research Staff Exchange Scheme (612681) of the EU 7th Framework Programme to R.G.O. The authors also thank Ana Carina Pamplona, Rafael Abe, and Marco Tulio Ramalho Zoratti for help with data collection. Corresponding author: Gerard Loughnane, Address: Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin 2, Ireland, Email: [email protected]; Phone: +3531 896 4543 Cite as: J. Neurosci ; 10.1523/JNEUROSCI.2340-17.2018 Alerts: Sign up at www.jneurosci.org/cgi/alerts to receive customized email alerts when the fully formatted version of this article is published. Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. Copyright © 2018 the authors 1 Antagonistic interactions between 2 microsaccades and evidence accumulation 3 processes during decision formation 4 Abbreviated title: Microsaccades disrupt evidence accumulation 1* 2 3 5 Gerard M. Loughnane , Daniel P. Newman , Sarita Tamang , Simon 3,4 1 6 P. Kelly & Redmond G. O’Connell 7 1 Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, 8 Dublin 2, Ireland. 9 2 School of Psychological Sciences and Monash Institute for Cognitive and Clinical 10 Neurosciences (MICCN), Monash University, Melbourne, VIC 3806, Australia. 11 3 Department of Biomedical Engineering, City College of the City University of New York. 12 4 School of Electrical and Electronic Engineering, University College Dublin, Dublin 4, Ireland. 13 Corresponding author: Gerard Loughnane 14 Address: Trinity College Institute of Neuroscience and School of Psychology, Trinity 15 College Dublin, Dublin 2, Ireland, 16 Email: [email protected]; Phone: +3531 896 4543 17 No. of pages: 42; No. of figures: 7. 18 Abstract word count: 157; Introduction word count: 649; Discussion word 19 count: 1154. 1 20 Acknowledgements: This study was supported by grants from the United States 21 National Science Foundation (BCS-1358955 to S.P.K. and R.G.O.), European 22 Research Council (63829 to R.G.O.), and the International Research Staff Exchange 23 Scheme (612681) of the EU 7th Framework Programme to R.G.O. The authors also 24 thank Ana Carina Pamplona, Rafael Abe, and Marco Tulio Ramalho Zoratti for help 25 with data collection. 26 27 28 29 30 31 32 33 34 35 36 37 2 38 Abstract 39 Despite their small size, microsaccades can impede stimulus detections if executed 40 at inopportune times. Although it has been shown that microsaccades evoke both 41 inhibitory and excitatory responses across different visual regions, their impact on 42 the higher-level neural decision processes that bridge sensory responses to action 43 selection has yet to be examined. Here we show that when human observers 44 monitor stimuli for subtle feature changes, the occurrence of microsaccades long 45 after (up to 800ms) change onset predicts slower reaction times, and that this is 46 accounted for by momentary suppression of neural signals at each key stage of 47 decision formation - visual evidence encoding, evidence accumulation, and motor 48 preparation. Our data further reveal that, independent of the timing of the change 49 events, the onset of neural decision formation coincides with a systematic inhibition 50 of microsaccade production, persisting until the perceptual report is executed. Our 51 combined behavioral and neural measures highlight antagonistic interactions 52 between microsaccade occurrence and evidence accumulation during visual 53 decision making tasks. 54 Significance statement 55 When fixating on a location in space, we frequently make tiny eye movements called 56 microsaccades. In the present study, we show that these microsaccades impede our 57 ability to make perceptual decisions about visual stimuli, and that this impediment 58 specifically occurs via the disruption of several processing levels of the sensorimotor 59 network; the encoding of visual evidence itself, the accumulation of visual evidence 3 60 towards a response, and effector-selective motor preparation. Furthermore, we show 61 that the production of microsaccades is inhibited during the perceptual decision, 62 possibly as a counteractive measure to mitigate their negative effect on behaviour in 63 this context. The combined behavioral and neural measures used in this study 64 provide strong and novel evidence for the interaction of fixational eye movements 65 and the perceptual decision making process. 66 Introduction 67 It is increasingly apparent that microsaccades – tiny fixational eye movements – play 68 a vital role in supporting perception (Hsieh and Tse, 2009; Martinez-Conde et al., 69 2013; Chen et al., 2015). However, these beneficial effects also come at a cost: to 70 ensure perceptual stability during movement of the retina, visual activity is disrupted 71 in the interval surrounding a microsaccade, leading to a transient increase in visual 72 thresholds and reaction times for stimuli appearing in that interval (Ditchburn, 1955; 73 Zuber and Stark, 1966; Beeler, 1967; Herrington et al., 2009; Hafed and Krauzlis, 74 2010; Tian and Chen, 2015). Thus, microsaccades are a potentially significant 75 contributor to behavioural variability on a wide range of perceptual tasks, a 76 commonly overlooked fact that has broad implications for basic and clinical research 77 on vision (Hafed et al., 2015). However, the precise neural mechanisms that mediate 78 microsaccadic perceptual suppression are not yet fully understood. 79 Neurophysiological investigations of this phenomenon have been recorded from 80 numerous visual areas under a variety of experimental contexts and while certain 81 areas exhibit excitatory modulations, others exhibit inhibitory modulations, and yet 4 82 others a combination of the two (Gur and Snodderly, 1987, 1997; Leopold and 83 Logothetis, 1998; Martinez-Conde et al., 2000, 2002; Dimigen et al., 2009; 84 Herrington et al., 2009; Chen et al., 2015; Tian and Chen, 2015). Further, while these 85 studies have focused primarily on the effects on sensory representations, the impact 86 of microsaccades on the higher-level processes that translate sensory information 87 into appropriate action has yet to be considered. 88 Convergent data from psychophysics, computational modelling and neurophysiology 89 highlight the central role of ‘decision variable’ signals in determining the timing and 90 accuracy of perceptual reports by accumulating sensory evidence over time up to an 91 action-triggering threshold (Shadlen and Kiani, 2013). Such accumulation-to-bound 92 dynamics have been demonstrated both in signals recorded non-invasively from the 93 human brain (Kelly and O'Connell, 2015), and in the spiking activity of certain 94 neuronal sub-populations within several sensorimotor regions of the monkey brain 95 (Roitman and Shadlen, 2002; Huk and Shadlen, 2005; Ratcliff et al., 2007). In two of 96 these regions, the lateral intraparietal area (LIP) and the superior colliculus, it has 97 been reported that microsaccades occurring around the time of stimulus onset result 98 in a brief suppression of activity (Herrington et al., 2009; Hafed and Krauzlis, 2010; 99 Chen et al., 2015, Chen and Hafed, 2017). However, these effects were not 100 observed specifically on neural signals reflecting evidence accumulation, and given 101 the heterogenous firing characteristics and breadth of functional roles associated 102 with these regions (Bisley and Goldberg, 2010; Gandhi and Katnani, 2011; Krauzlis 103 et al., 2013; Meister et al., 2013), it cannot be inferred whether and how 104 microsaccades may impact decision variable dynamics in particular. 5 105 Here, we sought to investigate the impact of microsaccades on perceptual decision 106 formation in the human brain. Although microsaccades have been studied in relation 107 to the visual responses they evoke over occipital areas (Dimigen et al., 2009; 108 Meyberg et al., 2015), no human study has yet established even basic aspects of 109 their impact on neural stimulus processing, such as the suppressive effects reported 110 in animal work. This is largely due to the technical challenges
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