Dependence of the Stimulus-Driven Microsaccade Rate Signature on 2 Visual Stimulus Polarity 3 4 Tatiana Malevich1,2,3*, Antimo Buonocore1,2, & Ziad M
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bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Dependence of the stimulus-driven microsaccade rate signature on 2 visual stimulus polarity 3 4 Tatiana Malevich1,2,3*, Antimo Buonocore1,2, & Ziad M. Hafed1,2 5 6 1Werner Reichardt Centre for Integrative Neuroscience, Tuebingen University, Tuebingen, Germany 7 72076 8 2Hertie Institute for Clinical Brain Research, Tuebingen University, Tuebingen, Germany 72076 9 3Graduate School of Neural and Behavioural Sciences, International Max-Planck Research School, 10 Tuebingen University, Tuebingen, Germany 72076 11 12 * Correspondence to: 13 [email protected] 14 15 Abbreviated title: 16 Black versus white stimulus onset effects on microsaccades 17 18 Corresponding author address: 19 Tatiana Malevich 20 Werner Reichardt Centre for Integrative Neuroscience 21 and 22 Hertie Institute for Clinical Brain Research 23 Otfried-Mueller Str. 25 24 Tuebingen, 72076 25 Germany 26 Phone: +49 7071 29 88821 27 28 29 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 30 Abstract 31 Microsaccades have a steady rate of occurrence during maintained gaze fixation, 32 which gets transiently modulated by abrupt sensory stimuli. Such modulation, 33 characterized by a rapid reduction in microsaccade frequency followed by a stronger 34 rebound phase of high microsaccade rate, is often described as the microsaccadic rate 35 signature, owing to its stereotyped nature. Here we investigated the impacts of 36 stimulus polarity (luminance increments or luminance decrements relative to 37 background luminance) and size on the microsaccadic rate signature. We presented 38 brief visual flashes consisting of large or small white or black stimuli over an otherwise 39 gray image background. Both large and small stimuli caused robust early 40 microsaccadic inhibition, but only small ones caused a subsequent increase in 41 microsaccade frequency above baseline microsaccade rate. Critically, small black 42 stimuli were always associated with stronger modulations in microsaccade rate after 43 stimulus onset than small white stimuli, particularly in the post-inhibition rebound phase 44 of the microsaccadic rate signature. Because small stimuli were also associated with 45 expected direction oscillations to and away from their locations of appearance, these 46 stronger rate modulations in the rebound phase meant higher likelihoods of 47 microsaccades opposite the black flash locations relative to the white flash locations. 48 Our results demonstrate that the microsaccadic rate signature is sensitive to stimulus 49 polarity, and they point to dissociable neural mechanisms underlying early 50 microsaccadic inhibition after stimulus onset and later microsaccadic rate rebound at 51 longer times thereafter. These results also demonstrate early access of oculomotor 52 control circuitry to sensory representations, particularly for momentarily inhibiting 53 saccade generation. 54 55 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 56 57 Keywords 58 Microsaccades; fixational eye movements; off responses; on responses; cueing; 59 saccadic inhibition 60 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 61 New and noteworthy 62 Microsaccades are small saccades that occur during gaze fixation. Microsaccade rate 63 is transiently reduced after sudden stimulus onsets, and then strongly rebounds before 64 returning to baseline. We explored the influence of stimulus polarity (black versus 65 white) on this “rate signature”. We found that small black stimuli cause stronger 66 microsaccadic modulations than white ones, but primarily in the rebound phase. This 67 suggests dissociated neural mechanisms for microsaccadic inhibition and subsequent 68 rebound in the microsaccadic rate signature. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 69 Introduction 70 Microsaccades occur occasionally during steady-state gaze fixation. When an 71 unexpected stimulus onset occurs under such steady-state conditions, as is the case 72 in a variety of behavioral experiments requiring maintained fixation (Hafed et al. 73 2015), stereotyped changes in microsaccade likelihood (and other properties) are 74 known to take place. Specifically, microsaccade likelihood, or rate per second, 75 abruptly decreases shortly after stimulus onset, remains near zero for a brief period 76 of time, and then momentarily rebounds to higher rates than before stimulus onset 77 (Bonneh et al. 2015; Buonocore et al. 2017a; Engbert and Kliegl 2003; Hafed and 78 Ignashchenkova 2013; Laubrock et al. 2005; Peel et al. 2016; Rolfs et al. 2008; Tian 79 et al. 2018; Valsecchi et al. 2007; White and Rolfs 2016). This pattern has been 80 termed the “microsaccadic rate signature” (Engbert and Kliegl 2003; Hafed and 81 Ignashchenkova 2013; Rolfs 2009; Rolfs et al. 2008; Scholes et al. 2015), owing to 82 its highly repeatable nature across many paradigms, and it is also related to the more 83 general phenomenon of saccadic inhibition reported for larger saccades (Bompas 84 and Sumner 2011; Buonocore and McIntosh 2008; Buonocore et al. 2016; Edelman 85 and Xu 2009; Reingold and Stampe 1999; 2004; 2002; 2003). 86 87 The neural mechanisms behind the microsaccadic rate signature, and saccadic 88 inhibition in general, are still being investigated. Neurophysiological perturbation 89 studies in the superior colliculus (SC), frontal eye fields (FEF), and primary visual 90 cortex (V1) have resulted in initial informative steps towards clarifying these 91 mechanisms. First, using a paradigm involving peripheral stimulus onsets, Hafed and 92 colleagues demonstrated that monkeys exhibit the same microsaccadic rate 93 signature as humans (Hafed et al. 2011). These effects persisted even after 94 thousands of trials performed by the same animals in the same tasks, confirming the 5 bioRxiv preprint doi: https://doi.org/10.1101/2020.05.23.112417; this version posted May 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 95 systematic nature of the effects. These authors then exploited the observation that 96 monkeys exhibit the same phenomenon as humans to perform invasive 97 neurophysiology; they reversibly inactivated portions of the SC topographic map 98 representing the locations of the appearing peripheral stimuli (Hafed et al. 2013). The 99 microsaccadic rate signature was virtually unaltered, whereas microsaccade 100 directions were significantly redistributed (Hafed et al. 2013), consistent with a 101 dissociation between the microsaccade rate signature and microsaccade direction 102 oscillations after stimulus onsets (Buonocore et al. 2017a; Hafed and 103 Ignashchenkova 2013; Tian et al. 2016). In follow up work, Peel and colleagues 104 extended these results by reversibly inactivating the FEF. They found that the early 105 inhibition was again unaltered, but, critically, the rebound phase of the microsaccadic 106 rate signature was affected (Peel et al. 2016); there were fewer post-inhibition 107 microsaccades than without FEF inactivation. In V1, lesions were found to affect 108 microsaccades in general, but the early inhibition after stimulus onset was generally 109 still present (Yoshida and Hafed 2017). Together with computational modeling (Hafed 110 and Ignashchenkova 2013; Tian et al. 2016), all of these initial results suggest that 111 there may be different components associated with the rate signature (e.g. inhibition 112 versus rebound) that are mediated by distinct neural circuits; the early inhibition is 113 clearly distinct from the later rebound that seems to particularly require frontal cortical 114 control. 115 116 That said, the microsaccadic rate signature in its entirety must be related to early 117 sensory responses, since the inhibition phase starts with very short latencies from 118 stimulus onset (approximately 60-70 ms in monkeys) (Hafed et al. 2011; Malevich et 119 al. 2020; Tian et al. 2018). It is, therefore, worthwhile to explore the effects of 120