Fictive reward signals in the anterior cingulate cortex

Abstract

The neural mechanisms supporting the ability to recognize and respond to fictive outcomes, outcomes of actions that one has not taken, remain obscure. We hypothesized that neurons in the anterior cingulate cortex (ACC), which monitors the consequences of actions and mediates subsequent changes in behavior, would respond to fictive reward information. We recorded responses of single neurons during performance of a choice task that provided information about the reward values of options that were not chosen. We found that ACC neurons signal fictive reward information and use a coding scheme similar to that used to signal experienced outcomes. Thus, individual ACC neurons process both experienced and fictive rewards.

Fig. 1

Task and recording location. A. Schematic of standard task. Fixation point and eight white squares appear; 500 ms after fixation, monkey chooses one target, and all targets change color, revealing their value. A half-second later, reward is given. B. Between trials, HV target either remains at the same position (60% chance) or moves to adjacent position (40% chance). C. MRI of monkey E. Recordings were made in ACC-sulcus.

Fig. 2

Fictive outcomes influence behavior. A. Histogram of distance between monkeys’ choices and optimal target, measured in squares clockwise. Dashed line: chance performance. B. Likelihood of choosing optimally increases as a function of both fictive and experienced reward outcome on previous trial. Black: trials following choice of LV. Gray: trials following choice of HV. C. Likelihood of switching to new target increases with size of fictive outcome on previous trial. D. and E. Likelihood and latency of immediately shifting gaze to HV location are not affected by fictive reward. F. Likelihood of choosing optimally is not influenced by a colored square presented during delay between trials (red line).

Fig. 3

ACC neurons signal both experienced and fictive rewards. A. Left: PSTH showing responses of example neuron following choice of HV target. Response grows with reward size. Vertical dashed lines indicate, successively, the time outcomes are revealed and reward is given. Shaded gray region indicates epoch used for bar graph showing average (+− 1 SE) response of neuron for each experienced reward size. B. Responses of same neuron for fictive rewards. Experienced reward was identical (100 μL) in all cases. C. Population response (n = 68 neurons) for experienced rewards, normalized to maximal firing rate for each neuron. D. Population response for fictive rewards.

Fig. 4

Neuronal responses signal both fictive rewards and subsequent adjustments in behavior. A. Firing rates following LV trials predict optimal choice on next trial for four of the six fictive outcomes. B. Neuronal responses to experienced rewards are identical on the trial that follows low (0 μL, red line) and high (>= 300μL, blue line) fictive outcomes, and thus do not signal reward prediction errors.