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Motivational Salience Guides Attention to Valuable and Threatening Stimuli: Evidence from Behavior and Functional Magnetic Resonance Imaging

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Motivational Salience Guides Attention to Valuable and Threatening Stimuli: Evidence from Behavior and Functional Magnetic Resonance Imaging Motivational Salience Guides Attention to Valuable and Threatening Stimuli: Evidence from Behavior and Functional Magnetic Resonance Imaging Haena Kim, Namrata Nanavaty, Humza Ahmed, Vani A. Mathur , and Brian A. Anderson Downloaded from http://direct.mit.edu/jocn/article-pdf/doi/10.1162/jocn_a_01769/1957795/jocn_a_01769.pdf by guest on 25 September 2021 Abstract ■ Rewarding and aversive outcomes have opposing effects on comparison of the neural correlates of value- and threat-based behavior, facilitating approach and avoidance, although we attentional capture after associative learning. Across multiple need to accurately anticipate each type of outcome to behave measures of behavior and brain activation, our findings over- effectively. Attention is biased toward stimuli that have been whelmingly support a motivational salience account of the learned to predict either type of outcome, and it remains an control of attention. We conclude that there exists a core mech- open question whether such orienting is driven by separate sys- anism of experience-dependent attentional control driven by tems for value- and threat-based orienting or whether there motivational salience and that prior characterizations of atten- exists a common underlying mechanism of attentional control tion as being value driven or supporting threat monitoring need driven by motivational salience. Here, we provide a direct to be revisited. ■ INTRODUCTION facilitate outcome-maximizing decisions (O’Doherty, Attention selectively processes perceptual information, 2004; Schultz, Dayan, & Montague, 1997). Through helping to ensure that stimuli relevant to survival and repetition, the caudate tail comes to encode stable value well-being are preferentially represented by the brain information (Kim & Hikosaka, 2013), which eventually (Corbetta & Shulman, 2002; Desimone & Duncan, 1995). contributes to incentive salience in which the reward- Traditionally, the allocation of limited attentional resources predictive stimuli automatically elicit an approach bias had been thought to be governed by task goals (Wolfe, (Berridge & Robinson, 1998). Cave, & Franzel, 1989) and physical salience (Theeuwes, The influence of prior experience shaped by aversive 2010). A newer construct, selection history, challenges this outcomes on the allocation of attention is beginning to dichotomy and suggests previous episodes of attentional be explored. Behaviorally, aversive outcomes bias atten- orienting are capable of independently biasing attention tion in a similar manner even when nonsalient and task in a manner that is neither top–down nor bottom–up irrelevant (Nissens, Failing, & Theeuwes, 2017; Schmidt, (Awh, Belopolsky, & Theeuwes, 2012). One component Belopolsky, & Theeuwes, 2015a, 2015b; Wentura, Müller, of selection history is reward history. Via associative & Rothermund, 2014), suggesting that the attentional learning, initially neutral stimuli come to predict reward system is primarily guided by motivational salience rather and thus acquire heightened attentional priority, conse- than a particular emotional valence. According to the quently capturing attention even when nonsalient and task motivational relevance model, both reward and aversive irrelevant (referred to as value-driven attentional capture; outcomes are important for survival (Gable & Harmon- e.g., Anderson, Laurent, & Yantis, 2011). Jones, 2010), hence eliciting automatic attentional The dopamine system is implicated in value-driven orienting that facilitates approach–avoidance behavior attentional capture. Increased dopamine release in the (Vuilleumier, 2005; LeDoux, 1996). basal ganglia (BG) leads to stronger attentional bias by Less is known about the neural mechanisms of atten- stimuli with reward history (Anderson et al., 2016, tional bias after aversive conditioning and whether there 2017), and in particular, the caudate tail responds prefer- exists a similar neural profile between value- and threat- entially to such stimuli (Anderson, Laurent, & Yantis, based orienting. Brain regions such as the striatum, 2014; Yamamoto, Kim, & Hikosaka, 2013). These findings ventral tegmental area, and substantia nigra process not corroboratetheliteratureontheroleofdopaminein only reward but also aversive outcomes (Liu, Hairston, formulating reward behavior; prediction error signals Schrier, & Fan, 2011; Jensen et al., 2003; Becerra, Breiter, Wise, Gonzalez, & Borsook, 2001). A subpopulation of dopamine neurons excites to both reward and aversive Texas A&M University outcomes (Bromberg-Martin, Matsumoto, & Hikosaka, © 2021 Massachusetts Institute of Technology Journal of Cognitive Neuroscience X:Y, pp. 1–21 https://doi.org/10.1162/jocn_a_01769 2010; Horvitz, 2000), suggesting aversive conditioning the CS+ or CS− color (see Figure 1). In Experiment 2, may bias attention in a manner similar to value-driven in a training phase, participants learned to associate attention, possibly via the nigrostriatal pathway that con- colors with either a reward (monetary gain), threat (un- trols oculomotor movement (Hikosaka, Nakamura, & avoidable electric shock), or no outcome (neutral). In a Nakahara, 2006; Hikosaka, Takikawa, & Kawagoe, test phase, a distractor square and a target circle were 2000). Such findings are consistent with the hypothesis presented simultaneously, one of which could appear that the attentional system is primarily guided by motiva- in either the previously reward- or threat-associated color tional salience. However, such regional overlap does not (see Figure 2). Experiment 1 provided an opportunity to necessitate a similar neural profile with respect to the characterize the neural correlates of automatic attentional control of attention. Indeed, reward and aversive out- processing of aversively conditioned stimuli. We found comes are also represented in dissociable neural systems that such attentional processing recruits brain regions that (Baliki, Geha, Fields, & Apkarian, 2010; Yacubian et al., are also implicated in value-driven attentional capture 2006). Alternatively, the two outcomes may be repre- with substantial apparent overlap, suggesting that atten- Downloaded from http://direct.mit.edu/jocn/article-pdf/doi/10.1162/jocn_a_01769/1957795/jocn_a_01769.pdf by guest on 25 September 2021 sented along a bipolar continuum; the same regions are tional bias toward reward and aversive outcomes involves excited after reward and suppressed after an aversive a common underlying mechanism. Motivated by these outcome (Becerra & Borsook, 2008; Delgado, Nystrom, findings, Experiment 2 afforded a direct comparison Fissell, Noll, & Fiez, 2000), consistent with the traditional between such neural correlates and the neural correlates view that dopamine neurons encode value signals of value-driven attention. If there exist genuinely disso- (Schultz et al., 1997). This differential encoding has con- ciable neural correlates between attentional bias toward sequences for action selection, in that reward promotes reward and aversive outcomes, then we would expect to approach and aversive outcomes promote inhibition or find a unique pattern of activation in response to distrac- avoidance (O’Doherty, 2004; Chen & Bargh, 1999). tors that signal reward and aversive outcomes. Such dissociable outcome representations could also have dissociable influences on the attention system, sug- gesting at least two separate mechanisms by which METHODS motivationally relevant stimuli capture attention. Experiment 1 Here, we present two experiments that examined the neural correlates of attentional bias after aversive condi- Participants tioning (Experiment 1) and the influence of reward and Thirty healthy participants (15 women; mean age = aversive outcomes on attentional bias (Experiment 2) 22.4 years) were recruited from the Texas A&M University using functional magnetic resonance imaging (fMRI). In community. All participants had normal or corrected- Experiment 1, participants completed a training phase to-normal visual acuity, normal color vision, no recent in which each of two differently colored circles was either history of chronic pain, and no current acute pain or followed by a mildly painful heat pulse applied to their injury and had not taken any pain medication for at least left forearm (CS+) or never paired with a heat pulse 3 days before the study. All procedures were approved (CS−). A subsequent test phase involved searching for by the Texas A&M University Institutional Review Board a shape-defined target among nonsalient distractors. and conformed with the principles outlined in the Sometimes, one of the distractors appeared in either Declaration of Helsinki. Figure 1. Sequence of events for a sample trial. (A) In the training phase, CS+ colored circles were followed by a heat pulse that gradually increased for 2 sec to reach the peak temperature, plateaued for 2 sec, and then gradually decreased back to the baseline for 2 sec. There were 30 trials in each run, half of which was CS+ trials. No heat stimulus was delivered on one third of the CS+ trials. (B) In the test phase, participants searched for a shape-defined target among nonsalient distractors. There were 60 trials in each run. On two thirds of the trials, one of the distractors appeared in either the CS+ color or CS− color (equally often). No CS distractor was present on the remaining trials. Participants completed five runs. 2 Journal of Cognitive Neuroscience Volume X, Number Y Figure 2. Sequence of events for a sample trial. (A) Each run of the training phase
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