Neural signatures of value comparison in human cingulate cortex during decisions requiring an effort-reward trade-off

Abstract Integrating costs and benefits is crucial for optimal decision-making. While much is known about decisions that involve outcome-related costs (e.g., delay, risk), many of our choices are attached to actions and require an evaluation of the associated motor costs. Yet how the brain incorporates motor costs into choices remains largely unclear. We used human functional magnetic resonance imaging during choices involving monetary reward and physical effort to identify brain regions that serve as a choice comparator for effort-reward trade-offs. By independently varying both options' effort and reward levels, we were able to identify the neural signature of a comparator mechanism. A network involving supplementary motor area (SMA) and the caudal portion of dorsal anterior cingulate cortex (dACC) encoded the difference in reward (positively) and effort levels (negatively) between chosen and unchosen choice options. We next modelled effort-discounted subjective values using a novel behavioural model. This revealed that the same network of regions involving dACC and SMA encoded the difference between the chosen and unchosen options' subjective values, and that activity was best described using a concave model of effort-discounting. In addition, this signal reflected how precisely value determined participants' choices. By contrast, separate signals in SMA and ventro-medial PFC (vmPFC) correlated with participants' tendency to avoid effort and seek reward, respectively. This suggests that the critical neural signature of decision-making for choices involving motor costs is found in human cingulate cortex and not vmPFC as typically reported for outcome-based choice. Furthermore, distinct frontal circuits ‘drive’ behaviour towards reward-maximization and effort-minimization. Significance Statement The neural processes that govern the trade-off between expected benefits and motor costs remain largely unknown. This is striking because energetic requirements play an integral role in our day-to-day choices and instrumental behaviour, and a diminished willingness to exert effort is a characteristic feature of a range of neurological disorders. We use a new behavioural characterization of how humans trade-off reward-maximization with effort-minimization to examine the neural signatures that underpin such choices, using BOLD MRI neuroimaging data. We find the critical neural signature of decision-making, a signal that reflects the comparison of value between choice options, in human cingulate cortex, whereas two distinct brain circuits ‘drive’ behaviour towards reward-maximization or effort-minimization.