Abstract

Although physical effort can impose significant costs on decision-making, when and how effort cost information is incorporated into choice remains contested, reflecting a larger debate over the role of sensorimotor networks in specifying behavior. Serial information processing models, in which motor circuits simply implement the output of cognitive systems, hypothesize that effort cost factors into decisions relatively late, via integration with stimulus values into net (combined) value signals in dorsomedial frontal cortex (dmFC). In contrast, ethology-inspired approaches suggest a more active role for the dorsal sensorimotor stream, with effort cost signals emerging rapidly after stimulus onset. Here we investigated the time course of effort cost integration using event-related potentials in hungry human subjects while they made decisions about expending physical effort for appetitive foods. Consistent with the ethological perspective, we found that effort cost was represented from as early as 100-250 ms after stimulus onset, localized to dorsal sensorimotor regions including middle cingulate, somatosensory, and motor/premotor cortices. However, examining the same data time-locked to motor output revealed net value signals combining stimulus value and effort cost approximately -400 ms before response, originating from sensorimotor areas including dmFC, precuneus, and posterior parietal cortex. Granger causal connectivity analysis of the motor effector signal in the time leading to response showed interactions between these sensorimotor regions and ventrolateral prefrontal cortex, a structure associated with adjusting behavior-response mappings. These results suggest that rapid activation of sensorimotor regions interacts with cognitive valuation systems, producing a net value signal reflecting both physical effort and reward contingencies. Although physical effort imposes a cost on choice, when and how effort cost influences neural correlates of decision-making remains contested. This dispute reflects a larger disagreement between cognitive neuroscience and ethology over the role of sensorimotor systems in behavior: are sensorimotor circuits merely implementing the late-stage output of cognitive systems, or engaged rapidly and interactively from early in decision-making? We find that, although early representation of effort cost is associated with sensorimotor regions, these signals are also integrated with cognitive stimulus value representations in the time leading up to motor response. These data suggest that sensorimotor networks interact dynamically with cognitive systems to guide decision-making, providing a first step toward reconciling differing perspectives on sensorimotor roles in valuation and choice.

Highlights

  • Physical effort, conceptualized as the cost associated with action to obtain an outcome (Rangel and Hare, 2010), often affects our Received Nov. 6, 2015; revised May 20, 2016; accepted May 25, 2016

  • This dispute reflects a larger disagreement between cognitive neuroscience and ethology over the role of sensorimotor systems in behavior: are sensorimotor circuits merely implementing the late-stage output of cognitive systems, or engaged rapidly and interactively from early in decision-making? We find that, early representation of effort cost is associated with sensorimotor regions, these signals are integrated with cognitive stimulus value representations in the time leading up to motor response

  • Tradeoffs between the intrinsic value of goods and the physical effort to obtain them are ubiquitous in daily life, researchers disagree on when and how effort cost is incorporated into decision-making at the neural level (Cisek and Kalaska, 2010; Padoa-Schioppa, 2011)

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Summary

Introduction

Physical effort, conceptualized as the cost associated with action to obtain an outcome (Rangel and Hare, 2010), often affects our Received Nov. 6, 2015; revised May 20, 2016; accepted May 25, 2016. When and how physical effort influences decision-making at the neural level is debated, reflecting tensions between cognitive neuroscience and ethological approaches over sensorimotor contributions to valuation and choice. Inspired by information processing models (Sternberg, 1969), cognitive researchers have proposed a serial progression from perceptual and cognitive stages to motor output, into which effort cost enters relatively late.

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