Journal of Vision (2019) 19(4):12, 1–14 1 The time course of different surround suppression mechanisms Department of Psychology, University of Washington, Seattle, WA, USA Department of Psychiatry and Behavioral Science, # Michael-Paul Schallmo University of Minnesota, Minneapolis, MN, USA $ Department of Psychology, University of Washington, Alex M. Kale Seattle, WA, USA Department of Psychology, University of Washington, # Scott O. Murray Seattle, WA, USA What we see depends on the spatial context in which it appears. Previous work has linked the suppression of Introduction perceived contrast by surrounding stimuli to reduced neural responses in early visual cortex. This surround The spatial context in which an image is seen suppression depends on at least two separable neural dramatically affects both how it is perceived and the mechanisms, ‘‘low-level’’ and ‘‘higher level,’’ which can underlying neural response. However, the link between be differentiated by their response characteristics. We the perceptual effects of spatial context and the used electroencephalography to demonstrate for the underlying neural mechanisms remains incomplete. first time that human occipital neural responses show Surround suppression is a spatial-context phenomenon evidence of these two suppression mechanisms. in which the presence of a surrounding stimulus reduces Eighteen adults (10 women, 8 men) each participated in the neural response to a center stimulus, compared to three experimental sessions, in which they viewed visual when that center image is viewed in isolation. This stimuli through a mirror stereoscope. The first session effect is clearly observed when stimuli are presented was used to identify the C1 component, while the both within and outside the classical receptive field of second and third comprised the main experiment. Event- neurons in primary visual cortex (V1), as measured by electrophysiology in animal models (Bair, Cavanaugh, related potentials were measured in response to center & Movshon, 2003; Cavanaugh, Bair, & Movshon, gratings either with no surround or with surrounding 2002a, 2002b; DeAngelis, Freeman, & Ohzawa, 1994; gratings oriented parallel or orthogonal, and presented Ichida, Schwabe, Bressloff, & Angelucci, 2007; Shush- in either the same eye (monoptic) or the opposite eye ruth, Ichida, Levitt, & Angelucci, 2009; Shushruth et (dichoptic). We found that the earliest component of an al., 2013; Walker, Ohzawa, & Freeman, 1999). Sur- event-related potential (C1; ;60 ms) was suppressed by round suppression is also observed in human visual surrounding stimuli, but that suppression did not depend perception; the perceived contrast or discriminability of on surround configuration. This suggests a suppression a center stimulus is reduced in the presence of a mechanism that is not tuned for relative orientation surround (Chubb, Sperling, & Solomon, 1989; Ejima & acting on the earliest cortical response to the target. A Takahashi, 1985; Petrov & McKee, 2006; Xing & later response component (N1; ;160 ms) showed Heeger, 2000, 2001; Yu, Klein, & Levi, 2001). stronger suppression for parallel and monoptic Perceptual surround suppression is thought to depend surrounds, consistent with our earlier psychophysical on suppressed neural responses in human visual cortex results and a second form of suppression that is (Schallmo, Grant, Burton, & Olman, 2016; Self et al., binocular and orientation tuned. We conclude that these 2016; Zenger-Landolt & Heeger, 2003). Indeed, stimuli two forms of surround suppression have distinct that produce perceptual surround suppression also response time courses in the human visual system, evoke suppressed neural responses in the human which can be differentiated using electrophysiology. occipital lobe, as measured by magneto- or electroen- Citation: Schallmo, M.-P., Kale, A. M., & Murray, S. O. (2019). The time course of different surround suppression mechanisms. Journal of Vision, 19(4):12, 1–14, https://doi.org/10.1167/19.4.12. https://doi.org/10.1167/19.4.12Received October 3, 2018; published April 5, 2019 ISSN 1534-7362 Copyright 2019 The Authors Downloaded from jov.arvojournals.orgThis work ison licensed 09/28/2021 under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. Journal of Vision (2019) 19(4):12, 1–14 Schallmo, Kale, & Murray 2 cephalography (EEG; Applebaum, Wade, Vildavski, level), which is binocular, stronger for parallel centers Pettet, & Norcia, 2006; Haynes, Roth, Stadler, & and surrounds (i.e., orientation selective), and greatly Heinze, 2003; Joo, Boynton, & Murray, 2012; Joo & attenuated following 30 s of adaptation with a dynamic Murray, 2014; Ohtani, Okamura, Yoshida, Toyama, & annular surround stimulus. This is consistent with Ejima, 2002; Vanegas, Blangero, & Kelly, 2015). current theories about the neural-circuit origins of Typically, greater suppression is observed for center surround suppression in V1; some amount of nonse- and surrounding stimuli that are more similar (e.g., lective suppression is thought to be inherited in a feed- parallel orientation). It has been suggested that forward manner from center–surround antagonism in surround suppression may serve a number of different the lateral geniculate nucleus (LGN), while horizontal functional roles in visual processing, including sup- connections within V1 and feedback from higher areas porting figure–ground segmentation (Poort et al., 2012; (e.g., V2, V4, MT) are thought to provide additional Poort, Self, van Vugt, Malkki, & Roelfsema, 2016; suppression that is selective for particular stimulus Roelfsema & de Lange, 2016), perceptual grouping features (e.g., orientation; Angelucci & Bressloff, 2006; (Joo et al., 2012; Joo & Murray, 2014), perceptual Nurminen & Angelucci, 2014). Psychophysical studies inference (Coen-Cagli, Kohn, & Schwartz, 2015), and in humans suggest that perceptual surround suppres- efficient coding of information (Vinje & Gallant, 2000). sion also depends on the same low- and higher level Although much is known about the phenomenon of mechanisms (Cai, Zhou, & Chen, 2008; Petrov & surround suppression, the neural mechanisms that give McKee, 2009). We have recently shown that suppres- rise to this effect remain imperfectly understood. sion of perceived contrast was stronger for parallel The time course of surround suppression may versus orthogonal surrounds viewed dichoptically (i.e., provide insight into the underlying neural processes. through a stereoscope, with the center appearing in one The pioneering work of Bair et al. (2003) showed that eye and the surround in the other), consistent with a surround suppression in macaque V1 has a latency of binocular, orientation-selective, higher level suppres- ;61 ms, slightly longer than that for the onset of a sion mechanism (Schallmo & Murray, 2016). We response to the center stimulus (;52 ms). Based on further showed that after adaptation in the surrounding their results, they concluded that a fast feedback region to a contrast-reversing grating, dichoptic sup- mechanism from higher visual areas (e.g., V2 or MT) pression was eliminated and monoptic suppression (i.e., may account for the observed time course of suppres- within the same eye) was equivalent for parallel and sion. Using magnetoencephalography, Ohtani et al. orthogonal surrounds. This second result was consis- (2002) found that the earliest measured response to a tent with a monocular, orientation-nonselective, low- center grating (;90 ms) was suppressed (but not level form of suppression. Using the stereoscope delayed) by the presence of a surrounding grating. permitted us to distinguish monocular versus binocular Haynes et al. (2003) used both magnetoencephalogra- processes, suggesting different stages of visual pro- phy and EEG to examine surround suppression, and cessing. Additional evidence of an interocular ‘‘contrast compared neural-response magnitudes to measures of normalization’’ mechanism that is orientation selective perceived contrast. They found suppression for collin- has been observed using functional MRI (Moradi & ear versus orthogonal center–surround configurations Heeger, 2009). However, to our knowledge, low- and in both early (;80 ms) and later (;130 ms) response higher level suppression have not been observed in components, but the later response was most closely human visual cortex using electrophysiology. Thus, associated with perception. From this early work and physiological evidence for these two suppression more recent studies (Chen, Yu, Zhu, Peng, & Fang, mechanisms in humans is lacking, and their particular 2016; Joo et al., 2012; Joo & Murray, 2014; Miller, effects across the neural-response time course remain Shapiro, & Luck, 2015; Vanegas et al., 2015), it is clear unknown. that surround suppression can be observed in the The current study sought to fill this gap in our earliest visually evoked responses from occipital areas knowledge by quantifying the signature of these two (e.g., V1). However, the precise neural origin of this putative surround-suppression mechanisms across time suppression (i.e., feed-forward, lateral interactions, or in the human visual system. We acquired event-related feedback) is not yet clear. potential (ERP) measurements in a paradigm we It has been shown that surround suppression developed previously (Schallmo & Murray, 2016) in an depends on at least two separable neural mechanisms attempt to distinguish low- and higher level processes with different physiological properties. Webb,