Dynamic routing of task-relevant signals for decision making in dorsolateral prefrontal cortex

Abstract

Neurons in the dorsolateral prefrontal cortex (DLPFC) encode a diverse array of sensory and mnemonic signals, but little is known about how this information is dynamically routed during decision making. We analyzed the neuronal activity in the DLPFC of monkeys performing a probabilistic reversal task where information about the probability and magnitude of reward was provided by the target color and numerical cues, respectively. The location of the target of a given color was randomized across trials and therefore was not relevant for subsequent choices. DLPFC neurons encoded signals related to both task-relevant and irrelevant features, but only task-relevant mnemonic signals were encoded congruently with choice signals. Furthermore, only the task-relevant signals related to previous events were more robustly encoded following rewarded outcomes. Thus, multiple types of neural signals are flexibly routed in the DLPFC so as to favor actions that maximize reward.

Figure 1

Behavioral task and performance. (a). Probabilistic reversal task, and magnitude combinations used (inset). (b) The proportion of trials in which the animal chose the same target color or location as in the previous trial after the previous choice was rewarded (win-stay) or unrewarded (lose-stay) (n=45 sessions in monkey O and 73 sessions in monkey U).

Figure 2

Population summary and single neuron examples for activity related to events in the previous trial. (a) Fraction of neurons significantly encoding outcomes, chosen locations, and chosen colors in the previous trial (n=226 neurons; 77 and 149 neurons from monkeys O and U, respectively). (b) Example neuron showing effect of outcome in the previous trial. (c) Example neuron showing effect of previously chosen location. (d) Example neuron showing effects of previously chosen color. Gray background, target period; shaded areas, ±SEM.

Figure 3

Population summary and single neuron examples for activity related to events in the current trial. (a) Fraction of neurons significantly encoding the chosen target location, chosen color, target color positions, and magnitudes in the current trial (n=226 neurons). (b) Example neuron showing effect of target position. (c) Example neuron showing effect of chosen color. (d) Example neuron showing effect of chosen location. (e) Example neuron encoding reward magnitude of the rightward target. Same format as in Fig. 2.

Figure 4

Population summary and single neuron examples related to interaction effects. (a) Fraction of neurons showing effects of previously rewarded location (PRL), previously chosen color and outcome, and their interaction corresponding to the high-value location (HVL) (n=226 neurons). (b) Example neuron showing encoding of HVL. (c) Example neuron encoding previously chosen color × previous outcome interaction. (d) Example neuron encoding PRL. Same format as in Fig. 2.

Figure 5

Congruent coding of HVL and choice. (a) Relationship between regression coefficients for HVL versus choice. (b) Relationship between regression coefficients for PRL versus choice (n=226 neurons). (c) Time course of first principal component (see Online Methods) related to choice, HVL, and PRL using signed regression coefficients. (d) Same result for unsigned regression coefficients. The arrow indicates chance levels based on 10,000 random shuffles (p<0.05).

Figure 6

Effects of reward on task-relevant and irrelevant signals in the DLPFC. (a) Example neuron encoding the high-value location (HVL), shown separately for leftward and rightward choices in the current trial. (b) Decoding accuracy for the current location of the previous chosen color, previous chosen location, and current chosen location, shown separately for previously rewarded and unrewarded trials (n=216 neurons that survived our criterion for cross-validation; see Online Methods). Shaded areas, ±SEM. The scatterplots in the bottom display the fraction of correct classifications for each neuron during the target period. Colors indicate whether neither, one, or both decoding analyses applied to previously rewarded and unrewarded were significantly above chance (p<0.05), and large symbols indicate that the difference between rewarded and unrewarded trials was statistically significant (z-test, p<0.05).