Abstract

Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-associated stimulus representations undergo plasticity in sensory cortex, thereby automatically capturing attention during early processing. To test this, we used magnetoencephalography to probe whether stimulus location and identity representations in sensory cortex are modulated by reward learning. We furthermore investigated the time course of these neural effects, and their relationship to behavioral VDAC. Male and female human participants first learned stimulus–reward associations. Next, we measured VDAC in a separate task by presenting these stimuli in the absence of reward contingency and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in posterior visual and parietal cortex from ∼260 ms after stimulus onset. This value modulation was related to the strength of participants' behavioral VDAC effect and persisted into subsequent target processing. Importantly, learned value did not influence cortical signatures of early processing (i.e., earlier than ∼200 ms); nor did it influence the decodability of stimulus identity. Our results suggest that VDAC is underpinned by learned value signals that modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual processing in cortex.SIGNIFICANCE STATEMENT Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus–reward associations, a phenomenon termed “value-driven attentional capture” (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity, which modulates early visual processing to capture attention. Although we find that learned value modulates spatial signals in visual cortical areas, an effect that correlates with VDAC, we find no relevant signatures of changes in early visual processing in cortex.

Highlights

  • Factors influencing selective attention have been traditionally categorized as stemming either from task demands or from physical salience

  • Choice accuracy was sensitive to the value difference between options, with a significant main effect of choice type [high vs zero (H-Z); high vs low (H-L); low vs zero (L-Z)] on accuracy (F(2,58) = 7.43, p = 0.006)

  • We found that this value modulation extended into the target epoch, consistent with the behavioral effects of value-driven attentional capture (VDAC) observed in the long stimulus-onset asynchrony (SOA) conditions (500 and 1000 ms)

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Summary

Introduction

Factors influencing selective attention have been traditionally categorized as stemming either from task demands (e.g., a red book will capture attention if one is searching for red books) or from physical salience (e.g., a red book among blue books will automatically capture attention; Desimone and Duncan, 1995; Egeth and Yantis, 1997; Beck and Kastner, 2009). Reward history (e.g., the learned association of a red logo with a rewarding experience) has been shown to play an important role in shaping attention (Awh et al, 2012; Anderson, 2013; Chelazzi et al, 2013). During a later “testing phase,” participants complete a new, formally unrelated task, which reuses the previously reward-associated stimuli (Anderson et al, 2011) These stimuli continue to capture attention even in the absence of any reward contingency, physical salience, or task relevance, a phenomenon termed value-driven attentional capture (VDAC; Raymond and O’Brien, 2009; Anderson et al, 2011; Theeuwes and Belopolsky, 2012; Chelazzi et al, 2014). VDAC is a prime example of how attention is influenced by prior experience; understanding its neural mechanisms is instrumental to bridging the fields of learning and attention (Anderson, 2016; Le Pelley et al, 2016; Failing and Theeuwes, 2018)

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