The electrocortical response to rewarding and aversive feedback: The reward positivity does not reflect salience in simple gambling tasks

Highlights

• RewP amplitude was more positive to desirable outcomes than undesirable outcomes.

• Safety from shock elicited a RewP comparable in magnitude to monetary gain.

• PCA revealed the RewP peaked earlier in the aversive vs. rewarding task versions.

• Findings support reward prediction error models of the RewP.

Abstract

The Reward Positivity (RewP) is an event-related potential (ERP) potentiated to monetary gains and reduced to monetary losses. Recently, competing data suggest that more salient outcomes elicit a positivity relative to less salient outcomes, regardless of valence. However, all previous work testing the impact of salience on the RewP have examined expected versus unexpected outcomes. In the current study, participants completed the same gambling task twice in which feedback was equally probable: in one condition, feedback indicated monetary gain or loss—and in the other condition, feedback indicated either safety or punishment from subsequent electric shock. Traditional ERP and principal component analysis (PCA)-derived measures confirmed that the RewP was more positive to feedback signaling monetary gain and safety from shock compared to feedback signaling monetary loss and punishment with shock. These results align with models in which the RewP indexes reward-related processes, including reward prediction error models. Potential explanations for salience-based effects on the RewP are discussed.

Introduction

For the past 20 years, ERP researchers have increasingly focused on the differentiation between positive and negative feedback to understand reward processing and learning (Miltner et al., 1997, Krigolson, n.d). Across time estimation (Miltner et al., 1997, Becker et al., 2014), reinforcement learning (Baker and Holroyd, 2008, Holroyd et al., 2011), and simple gambling tasks (Gehring and Willoughby, 2002, Holroyd et al., 2004, Holroyd et al., 2006, Proudfit, 2015), studies have consistently observed a relative negativity that peaks approximately 300 ms following feedback indicating bad compared to good outcomes. This relative negativity has been referred to as the feedback error-related negativity (Miltner et al., 1997, Holroyd and Coles, 2002, Holroyd et al., 2006, Nieuwenhuis et al., 2004), feedback negativity (Yeung and Sanfey, 2004), feedback related negativity (Cohen et al., 2007, Hajcak et al., 2006, Liu et al., 2014), and the medial frontal negativity (Gehring and Willoughby, 2002). More recent accounts suggest that this negativity may be a N200 to unexpected events that require increased need for cognitive control (Holroyd, 2004, Holroyd et al., 2008), and that this N200 is suppressed by a reward-sensitive positivity on reward trials (Holroyd et al., 2008). When conceptualized as a relative positivity following reward, several authors have suggested naming the ERP accordingly, either as the feedback correct-related positivity or the reward positivity (RewP; Holroyd et al., 2008, Proudfit, 2015).

Several lines of evidence suggest rewards drive the ERP difference between positive and negative feedback, including experimental manipulations (Holroyd et al., 2006, Holroyd et al., 2008, Kujawa et al., 2013), principal components analysis (PCA) of the ERP waveform (Foti et al., 2011, Weinberg et al., 2014, Liu et al., 2014, Carlson et al., 2011), and correspondence of the RewP to both reward-related behavioral (Bress and Hajcak, 2013) and neural measures derived from fMRI (Carlson et al., 2011, Becker et al., 2014, Foti et al., 2014). Collectively, these data suggest a positive potentiation in the ERP following rewards that is reduced or absent on non-reward trials.

Functionally, the RewP is thought to reflect a reward prediction error signal, which codes whether outcomes are better or worse than expected (Holroyd and Coles, 2002, Holroyd et al., 2008, Walsh and Anderson, 2012, Sambrook and Goslin, 2015). Consistent with this view, the RewP is larger when rewards are unexpected (Holroyd et al., 2011) and larger in magnitude (Sambrook and Goslin, 2015). While there is much evidence to suggest that the RewP is a reward-related modulation of the ERP, recent studies have provided evidence for the possibility that the RewP instead reflects a salience prediction error (SPE) signal. That is, the RewP may instead differentiate high- from low-salience events, regardless of valence. In this view, rewards might elicit a RewP because reward is more salient than non-reward.

In particular, two studies have found more positive ERP responses to feedback indicating aversive outcomes relative to feedback signaling the omission of aversive outcomes (Soder and Potts, n.d, Talmi et al., 2013). In terms of their experimental design, both studies presented participants with an initial cue that induced expectations regarding the likelihood of the outcome on each trial; following this cue (S1), participants were presented with feedback (i.e., the S2) that indicated expected or unexpected reward, or with feedback that indicated an expected or unexpected punishment (i.e., electric shocks in Talmi et al., 2013; noise blasts in Soder & Potts, this issue). Both Talmi and colleagues, as well as Soder and Potts, found that the S2 indicating unexpected reward elicited a positivity in the waveform relative to unexpected non-reward; however, both studies also found that the S2 signaling unexpected punishment also elicited a positivity relative to unexpected punishment omission (Talmi et al., 2013, Soder and Potts, n.d). The notion that unexpected punishment would elicit a RewP is inconsistent with reward-related accounts and suggests instead that a RewP may be elicited by salient outcomes.

Heydari and Holroyd (2016) have reported competing findings from a study in which participants navigated a virtual T maze and received feedback in rewarding and aversive conditions. Feedback indicated absence or presence of monetary reward in the rewarding condition, and absence or presence of small shock in the aversive condition. They found the RewP to be more positive to feedback indicating receipt of monetary reward as compared to its omission, and to feedback indicating omission of shock relative to impending shock. Thus, this study utilized a similar paradigm to those from Talmi et al. (2013) and Soder & Potts (current issue) by employing rewarding and aversive conditions, however, their results demonstrated the RewP tracked feedback valence rather than salience.

In the studies from Talmi et al. (2013) and Soder and Potts (current issue), the S1–S2 design was used to induce expectations regarding outcomes. However, participants never made choices—there was no response requirement in either the Talmi et al., or Soder and Potts experiments. This is particularly relevant given the fact that experimental results suggest that the RewP is maximized by feedback that follows volitional choice (Walsh and Anderson, 2012, Yeung and Sanfey, 2004). Moreover, many studies that have examined the RewP do so in the context of simple guessing tasks in which reward and loss are equiprobable on each trial (Gehring and Willoughby, 2002, Holroyd et al., 2004, Holroyd et al., 2006, Proudfit, 2015).

The current study employed a simple guessing task and within-subject design to examine whether feedback that signaled impending shock or safety would elicit a RewP. Subjects were administered two identical versions of a guessing task: a monetary version in which choices led to either monetary gain or loss—and an aversive version in which choices led to either safety from shock or punishment with shock. In this way, we employed identical features as Talmi and colleagues and Soder and Potts, however, feedback followed participant choices and were equiprobable on each trial. Traditional and principal component analysis (PCA)-derived factors were analyzed to assess the impact of outcome on ERPs. If the more rewarding outcomes (i.e., monetary gain and safety from shock) elicit a relative positivity compared to non-rewarding outcomes (i.e., monetary loss and punishment), the data would support the role of the RewP in reward-related process. If more salient outcomes (i.e., monetary gain and punishment) elicit a positivity relative to less salient outcomes (i.e., monetary loss and safety from shock), the data would support the SPE model and sensitivity of the RewP to salient outcomes.