Research Report: Regular Manuscript Physical salience and value-driven salience operate through different neural mechanisms to enhance attentional selection https://doi.org/10.1523/JNEUROSCI.1198-19.2020 Cite as: J. Neurosci 2020; 10.1523/JNEUROSCI.1198-19.2020 Received: 21 May 2019 Revised: 10 May 2020 Accepted: 13 May 2020 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2020 the authors 1 Title: Physical salience and value-driven salience operate through different neural mechanisms 2 to enhance attentional selection 3 Abbreviated title: Physical salience versus value-driven salience 4 Author names and affiliations: Matthew D. Bachman*, Lingling Wang (⦻⧢⧢)*, Marissa L. 5 Gamble, Marty G. Woldorff 6 Center for Cognitive Neuroscience, Duke University, Durham, NC, 27708 7 *Equal contribution 8 Corresponding author: Marty G. Woldorff; [email protected]; Center for Cognitive 9 Neuroscience, Duke University, Box 90999, Durham, NC 27708 10 Number of pages: 31 11 Number of figures: 6 12 Number of tables: 4 13 Number of words for Abstract: 250 14 Number of words for Introduction: 700 15 Number of words for Discussion: 1538 16 Conflict of Interest: The authors declare no competing financial interests. 17 Acknowledgements: This work was supported by R56-NS051048 from the National Institutes 18 of Health awarded to M.G.W. Lingling Wang is now affiliated with Carl Zeiss (Shanghai) Co. 19 Ltd. Marissa L. Gamble is now affiliated with True Fit Corporation PHYSICAL SALIENCE VERSUS VALUE-DRIVEN SALIENCE 2 20 Abstract 21 Previous studies have indicated that both increased physical salience and increased 22 reward-value salience of a target improves behavioral measures of attentional selection. It is 23 unclear, however, whether these two forms of salience interact with attentional networks through 24 similar or different neural mechanisms, and what such differences might be. We examined this 25 question by separately manipulating both the value-driven and physical salience of targets in a 26 visual search task while recording response times (RTs) and event-related potentials (ERPs), 27 focusing on the attentional-orienting-sensitive N2pc ERP component. Human participants of 28 both sexes searched arrays for targets of either a high-physical-salience color or one of two low- 29 physical-salience colors across three experimental phases. The first phase (“baseline”) offered no 30 rewards. RT and N2pc latencies were shorter for high-physical-salience targets, indicating faster 31 attentional orienting. In the second phase (“equal-reward”) a low monetary reward was given for 32 fast correct responses for all target types. This reward context improved overall performance, 33 similarly shortening RTs and enhancing N2pc amplitudes for all target types, but with no change 34 in N2pc latencies. In the third phase (“selective-reward”) the reward rate was made selectively 35 higher for one of the two low-physical-salience colors, resulting in their RTs becoming as fast as 36 the high-physical-salience targets. Despite the equally fast RTs, the N2pc’s for these low- 37 physical-salience, high-value targets remained later than for high-physical-salience targets, 38 instead eliciting significantly larger N2pc’s. These results suggest that enhanced physical 39 salience leads to faster attentional orienting, but value-driven salience to stronger attentional 40 orienting, underscoring the utilization of different underlying mechanisms. 41 42 2 PHYSICAL SALIENCE VERSUS VALUE-DRIVEN SALIENCE 3 43 Significance Statement 44 Associating relevant target stimuli with reward value can enhance their salience, 45 facilitating their attentional selection. This value-driven salience improves behavioral 46 performance, similar to the effects of physical salience. Recent theories, however, suggest that 47 these forms of salience are intrinsically different, although the neural mechanisms underlying 48 any such differences remain unclear. This study addressed this issue by manipulating the 49 physical and value-related salience of targets in a visual search task, comparing their effects on 50 several attention-sensitive neural-activity measures. Our findings show that, whereas physical 51 salience accelerates the speed of attentional selection, value-driven salience selectively enhances 52 its strength. These findings shed new insights into the theoretical and neural underpinnings of 53 value-driven salience and its effects upon attention and behavior. 54 55 56 57 58 59 60 61 62 3 PHYSICAL SALIENCE VERSUS VALUE-DRIVEN SALIENCE 4 63 Introduction 64 A rapidly expanding body of research has begun documenting how attention is biased 65 towards reward-associated features, a phenomena known as value-driven attentional capture 66 (VDAC; for reviews, see Anderson et al. 2011b; Chelazzi et al. 2013; Failing & Theeuwes, 67 2018). This biasing of attention tends to be involuntary and non-strategic (Hickey et al., 2010; 68 Hickey & van Zoest, 2012), which means its impact upon behavior can vary substantially 69 depending on the context. If the reward-associated feature is tied to a task-relevant parameter 70 then it can facilitate the shift in attention towards this item, improving behavioral performance 71 (Failing & Theeuwes, 2014; Raymond & O'Brien, 2009). However, if it is tied to a task- 72 irrelevant parameter, then it can draw attention away, ultimately impairing behavioral 73 performance (Anderson et al., 2011b; Theeuwes & Belopolsky, 2012). This suggests that 74 associating a stimulus with a reward enhances its pertinence to the visual system, increasing its 75 overall salience in some key ways. 76 VDAC’s variable impact upon behavioral performance bears considerably similarity to 77 that of a different modulator of attention: physical salience. Physical salience is generated from 78 the distinctiveness of the stimulus’s physical properties (e.g., color, shape) with respect to other 79 objects in a scene (Theeuwes, 1994, 2010; Itti & Koch, 2001; Wolfe, 2007). These distinctive 80 physical features capture attention quickly and automatically; targets imbued with high physical 81 salience relative to its surrounding neighbors generate faster response times (RTs) and the onset 82 of electrophysiological markers of visual selection occur earlier in time (Luck et al., 2006; 83 Töllner et al., 2011). Conversely, salient distractors can slow RTs and generate later neural 84 markers of visual selection (Theeuwes 1991, 1992; Hickey et al. 2006). 4 PHYSICAL SALIENCE VERSUS VALUE-DRIVEN SALIENCE 5 85 In summary, both physical salience and salience formed from reward value (i.e. value- 86 driven salience) share many important characteristics. Cognitively, objects high in either type of 87 salience appear to gather attention more rapidly and involuntarily, and their behavioral 88 consequences are both dependent upon the task-relevance of the salient item. Although these 89 similarities have been noted in early reports of VDAC research (Hickey et al., 2010), various 90 theoretical accounts of these processes have argued that they are distinct phenomena (Awh et al., 91 2012), suggesting there are key differences at some level in their underlying neural mechanisms. 92 This idea is supported by findings that value-driven salience is related to fMRI activity not only 93 within the visual cortex but in the striatum as well (Anderson 2014; Hickey & Peleen, 2015). A 94 recent review highlighted that value-driven salience does involve an extended network of brain 95 regions, but also suggested that it should ultimately modulate attentional allocation in an 96 analogous, bottom-up way just as if it were more physically salient (Anderson 2019) . Yet, to our 97 knowledge, this view has yet to be specifically and directly tested. 98 Most prior investigations of value-driven salience or physical salience were designed to 99 control for one form of salience while manipulating the other, so that changes in behavior could 100 be appropriately attributed to the specific type of salience of interest. Consequently, few studies 101 have compared the impact of these two forms of salience upon attentional allocation. A handful 102 of behavioral studies have begun investigating these differences, and have generally concluded 103 that both forms of salience have independent contributions to behavior (Anderson et al., 2011a; 104 Wang et al., 2013; Gong & Liu, 2018). While this provides some support to the idea that the 105 mechanisms by which these forms of salience do differ, the lack of corresponding neuroscience 106 studies means the exact differences in the underlying neural mechanisms remains unknown. 5 PHYSICAL SALIENCE VERSUS VALUE-DRIVEN SALIENCE 6 107 The current study was designed to directly compare the effects of physical salience and 108 value-driven salience upon visual selection, while measuring the underlying neural processes. To 109 this end, we employed a visual search task composed of uniquely colored pop-out targets in an 110 array and manipulated both the physical salience and value-driven salience of the targets by 111 varying the physical distinctiveness of the target color and its associated monetary reward value, 112 respectively. Scalp EEG was recorded