Neural representations of confidence emerge from the process of decision formation during perceptual choices

Highlights

• Choice confidence emerges as early as the decision process itself.

• Choice confidence is reflected in the accumulation rate of decision evidence.

• Source generators for choice confidence in lateral prefrontal and parietal cortices.

• Metacognitive appraisal could depend on early signatures of confidence.

Abstract

Choice confidence represents the degree of belief that one's actions are likely to be correct or rewarding and plays a critical role in optimizing our decisions. Despite progress in understanding the neurobiology of human perceptual decision-making, little is known about the representation of confidence. Importantly, it remains unclear whether confidence forms an integral part of the decision process itself or represents a purely post-decisional signal. To address this issue we employed a paradigm whereby on some trials, prior to indicating their decision, participants could opt-out of the task for a small but certain reward. This manipulation captured participants' confidence on individual trials and allowed us to discriminate between electroencephalographic signals associated with certain-vs.-uncertain trials. Discrimination increased gradually and peaked well before participants indicated their choice. These signals exhibited a temporal profile consistent with a process of evidence accumulation, culminating at time of peak discrimination. Moreover, trial-by-trial fluctuations in the accumulation rate of nominally identical stimuli were predictive of participants' likelihood to opt-out of the task, suggesting that confidence emerges from the decision process itself and is computed continuously as the process unfolds. Correspondingly, source reconstruction placed these signals in regions previously implicated in decision making, within the prefrontal and parietal cortices. Crucially, control analyses ensured that these results could not be explained by stimulus difficulty, lapses in attention or decision accuracy.

Introduction

Imagine running in the park on a rainy day, trying to discern whether the person across the lawn is an old friend. The decision to keep concentrating on your stride or change directions to go greet them depends on your level of confidence that it is really them. Choice confidence is crucial not only for such mundane tasks, but also for more biologically and socially complex situations. It provides a probabilistic assessment of expected outcome and can play a key role in how we adjust in ever-changing environments, learn from trial and error, make better predictions, and plan future actions.

In recent years, systems and cognitive neuroscience started to examine the neural correlates underlying perceptual decision making. As a result, many monkey neurophysiology (Gold and Shadlen, 2007, Kim and Shadlen, 1999, Mazurek et al., 2003, Newsome et al., 1989, Shadlen et al., 1996, Shadlen and Newsome, 2001), human neuroimaging (Cheadle et al., 2014, Heekeren et al., 2004, Heekeren et al., 2006, Heekeren et al., 2008, Ho et al., 2009, Ploran et al., 2007, Tosoni et al., 2008), and human electrophysiology (de Lange et al., 2010, Donner et al., 2007, Donner et al., 2009, O'Connell et al., 2012, Philiastides et al., 2006, Philiastides and Sajda, 2006, Ratcliff et al., 2009, Wyart et al., 2012) experiments provided converging support that perceptual decisions are characterized by a noisy temporal accumulation of sensory evidence which culminates when an observer commits to a choice. Despite this progress, however, it remains unclear how confidence is represented in the human brain and what its relationship is with the decision process itself.

Current theoretical and experimental accounts have regarded confidence as a meta-cognitive event (i.e. an epiphenomenon of the decision process) that relies on new information arriving beyond the decision point (Fleming et al., 2012, Pleskac and Busemeyer, 2010, Yeung and Summerfield, 2012). Conversely, little has been done in the way of exploring whether confidence might emerge earlier in the decision process and before one commits to a choice. Evidence for the latter has recently emerged from a limited number of animal studies (Kepecs et al., 2008, Kiani and Shadlen, 2009, Shadlen and Kiani, 2013), proposing that choice confidence in perceptual judgments might be an inherent property of the decision process itself and that the same neural generators involved in evidence accumulation also encode choice confidence. To date, it remains unclear whether confidence forms an integral part of the decision process itself and whether it emerges from the same neural generators involved in accumulating evidence for the decision. Similarly, it is unknown whether confidence is reflected in the rate of evidence accumulation itself.

To address these open questions, we collected electroencephalography (EEG) data during a binary, delayed-response, task in which correct responses were rewarded with monetary incentives. Importantly, on a random half of trials and after forming a decision, participants were given the option to opt out of the task for a smaller but sure reward (a form of post-decision wager (Kiani and Shadlen, 2009)). We expected participants to waive the sure reward when they were certain of their choice, and select it otherwise. This in turn allowed us to use a multivariate single-trial classifier to discriminate between certain-vs.-uncertain trials to identify the temporal characteristics of the neural correlates of choice confidence. Importantly, additional control analyses were carried out to ensure that confidence-related effects could not be explained by stimulus difficulty or trial-by-trial changes in attention.