Stimulus Visibility Reflected in Microsaccade Activity Jie Cui 1, Melanie Wilke 2, Nikos Logothetis 3, David Leopold 2, Hualou Liang 1 1 School of Health Information Sciences, University of Texas Health Science Center at Houston, Houston, TX, USA 2 UCNI/National Institute of Mental Health MSC-4400, 49 Convent Bethesda, MD, USA 3 Max Planck Institute for Biological Cybernetics, Spemmanstraße 38, 72076, Tübingen, Germany University of Texas Health Science Center at Houston E-contact:: Background Methods Average MS Rates Reflect Perceptual States Summary and Conclusion Our eyes are never still, but continuously move even at the moment of fixation. Microsaccades (MSs) are the largest “fixational” eye movements that are rapid and involuntary jerks of the eyes (generally < 1°) [1]. Recent behavior and neurophysiologic evidences suggest their fundamental role in visual processing [2]. However, whether microsaccades facilitate a bottom-up flow of information leading to microsaccade-driven perception, or their behavior is primarily affected by a top-down influence from higher cognitive activity keeps unsolved. If microsaccades play a role in visual perception and their behavior pattern is also influenced by cognitive states of perception, we hypothesize that the behavioral characteristics of microsaccades should be highly correlated with the perceptual states during visual suppression and other multistable perception. Reference Visual Perception Modulates MS Rate Evolution MS Direction Affected by Target Visibility I. Visual Stimulus To test the hypothesis, we analyzed microsaccade behavior observed in three non-human primates (ER, WA and DA) experiencing general flash suppression (GFS) [3]. The figure depicts the specific stimulus sequence that was used to induce a complete disappearance of a salient target (red disk) after surround onset (white dots). A typical trial started with a warning tone to cue the monkey to maintain fixation at a small central disk (yellow dots) ms before surround onset, the target was turned on at a parafoveal location on the screen. In the sessions included in this analysis, all the targets were displayed in the lower half of the screen. The monkey had to hold a level as long as the target was visible and to release it as soon as the target was invisible. The probability of perceptual suppression of the target was adjusted to about 50%. Trials were grouped into three classes: “visible”, “invisible” and “physical disappearance” trials. In physical disappearance trials the targets were removed physically from the screen. Eye movements were identified as microsaccades if peak velocity exceeded 4 standard deviation of the mean with an amplitude less than 36 arcmin (diameter of the fixation window) and duration longer than 8 ms. Figure shows a typical example of eye positions after target onset. Detected microsaccades marked in red are superimposed on the vertical (green) and horizontal (blue) traces. Vertical red dotted lines indicate the onset of microsaccades. More details of one microsaccade are shown in inlet. II. Microsaccade Detection I. Average Rates II. Other Average Parameters Average microsaccade rate after surround on under “invisible” condition is significantly lower than that under “visible” condition, but not that under “physical disappearance”, which indicates that microsaccade rate is strongly influenced by target visibility However, there is no significant difference in the parameters of amplitude, duration and peak velocity for the three perceptual conditions. Therefore, these parameters in general are not sensitive to different perceptual states. Evolution of microsaccade rate was examined as a function of perceptual states. The averaged (Panel A) and the individual variation (Panels B – D) from the three monkeys shows that: An initial strong inhibition of rate irrespective to perceptual conditions In “visible” trials the microsaccade rate promptly rebound to pre-surround-onset level in about 250 ms posterior to the rate minimum In “invisible” trials the rate remains low, reaching pre-onset level later than that in the visible trials In “physical disappearance” trials the rate generally follow that in “invisible” trials. The results suggest that the perceptual suppression of the target is unlikely caused by the reduction of microsaccade rate. The evolution of microsaccade rate is highly modulated by the visual perception of the target. The polar histogram of microsaccade direction reveals a higher “toward-target” (downward) tendency (76.4%) in the visible condition than that (60.5%) in the invisible condition. In the control condition of “physical dis- appearance” the proportion of downward microsaccades is 66.6%. The left figure shows the dynamics of directional frequency per condition, which is the difference between the rate of “toward- target” microsaccades and the rate of “opposite-to-target” ones. The results suggest that more toward-target microsaccades were generated when the target was visible. When the target was in- visible (subjectively or physically), the microsaccades to either directions were generated at an approximately equal rate. Specific patterns of oculomotor activity reflect different states of visibility in GFS experiments  During the perceptual disappearance of a salient target, the microsaccade activities are strongly inhibited, while the activities are promptly recovered when the target keeps visible.  More microsaccades are directed to the target than to the opposite direction when it is visible. When the target is invisible, microsaccades are generated at an approximately equal rate to both directions.  Patterns of microsaccade activities in “physical disappearance” condition follow closely the patterns in “invisible” condition. Therefore, microsaccade absence unlikely directly causes the target suppression. Thus, microsaccade behavior is highly correlated with the perceptual state of target visibility and primarily driven by higher cognitive activity. Microsaccadic rate and direction can be reliable indicators of the inner perceptual states. [1] Martinez-Conde, S., Macknik, S.L. & Hubel D.H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience, 5(3), [2] Leopold, D.A., & Logothetis, N.K. (1998). Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Experimental Brain Research, 123(3), [3] Wilke, M., Logothetis, N.K., & Leopold, D.A. (2006). Local field potential reflects perceptual suppression in monkey visual cortex. Proceedings of the National Academy of Science of the United States of America, 103(46), Acknowledgment: NIH R01 MH072034, the Max Planck Society & NSERC Postdoctoral Fellowship to J.C.