Prelimbic Cortical Neurons Track Preferred Reward Value and Reflect Impulsive Choice during Delay Discounting Behavior

Abstract

In delay discounting, individuals discount the value of a reward based on the delay to its receipt. The prelimbic cortex (PrL) is heavily interconnected with several brain regions implicated in delay discounting, but the specific contributions of the PrL to delay discounting are unknown. Here, we used multineuron electrophysiological recording methods in Long-Evans male (n = 10) and female (n = 9) rats to characterize the firing dynamics of PrL neurons during discrete cue and lever press events in a delay discounting task. Rats' initial preference for the large reward decreased as delays for that outcome increased across blocks, reflecting classic discounting behavior. Electrophysiological recordings revealed that subgroups of neurons exhibited phasic responses to cue presentations and lever presses. These phasic neurons were found to respond to either large/delay, small/immediate, or both trial types and the percentage of these neurons shifted across blocks as the expected value of the reward changed. Critically, this shift was only seen during trials in which animals could choose their preferred option (free choice trials) and not during trials where animals could choose only one option (forced choice trials). Further, this shift was dependent on rats' inherent impulsivity because high impulsive rats demonstrated a greater percentage of small/immediate-responsive neurons as the task progressed. Collectively, these findings suggest a unique role for the PrL in encoding reward value during delay discounting that is influenced by individual differences in impulsivity.SIGNIFICANCE STATEMENT In delay discounting, individuals discount the value of a reward based on the delay to its receipt. Here, we used electrophysiology to investigate the role of the prelimbic cortex (PrL) in this process. We found that subsets of neurons shifted activity as a function of the changing expected delay and reward magnitude, but this shift was only evident during trials in which animals could choose their preferred option. Further, this dynamic neural activity depended on rats' inherent impulsivity, with impulsive rats exhibiting a stronger neural shift toward the immediate reward as the task progressed. These findings suggest a role for the PrL in encoding reward value during delay discounting that is influenced by goal-directed context and individual differences in impulsivity.

Keywords: accumbens; behavior; decision making; impulsivity; prefrontal; prelimbic.

Figure 1.

Delay discounting task and behavior. A, On forced choice delay trials (left), a 5 s cue predicted the opportunity to press a lever for a large reward after a period of delay. On forced-choice immediate trials (middle), the other cue light predicted the opportunity to respond for a small reward delivered immediately. On free choice trials (right), both cue lights predicted the opportunity to choose between large delayed or small immediate rewards. B, Free choice behavior in male and female rats during the delay discounting task. Responses for the large reward decreased as delay to reward increased. C, Accuracy (percentage correct responses) for each block and across all rats. *p < 0.05.

Figure 2.

PrL cortical neurons respond to cue presentations. A, Peri-event histograms (PEHs) of representative neurons exhibiting an excitation (left) or an inhibition (right) in firing rate during cue presentations. Data are aligned to cue onset (time 0, dashed line); cue duration is indicated by horizontal lines below PEHs. B, Pie charts illustrating proportion of neurons that exhibited phasic responses during free choice cue presentations across blocks based upon whether the rat subsequently chose the large/delay reward (top row) or small/immediate reward (bottom row).

Figure 3.

PrL cortical neurons respond to lever press. A, Peri-event histograms (PEHs) of representative neurons exhibiting an excitation (left) or an inhibition (right) in firing rate relative to lever press responses. Data are aligned to lever press (time 0, dashed line). B, Pie charts illustrating the proportion of neurons that exhibited phasic responses during free choice lever presses for either the large/delay reward (top row) or the small/immediate reward (bottom row).

Figure 4.

Distinct subsets of PrL neurons selectively track information related to discounted choice. Top, Peri-event histogram (PEH) of a representative neuron exhibiting excitatory firing during cue presentations only during the large/delay (left), but not during small/immediate cue presentations (right). Data are aligned to cue presentation (time 0, dashed line); duration is indicated by horizontal line below PEHs. Middle, PEH of a representative PrL neuron exhibiting excitatory activity to cues during small/immediate trials (right) not during large/delay cue presentations (left). Bottom, PEHs of a representative neuron that exhibited excitatory activity to both large/delay (left) and small/immediate (right) cue presentations.

Figure 5.

Proportions of event-related (cue, press) responsive neurons dynamically decline across free choice (left) but not forced choice (right) blocks. A, Proportion of phasically active responsive neurons to free choice cue presentations. B, Proportion of phasically active responsive neurons to forced choice cue presentation. C, Proportion of phasically responsive neurons to free choice lever press. D, Proportion of phasically responsive neurons to forced choice lever press. *p < 0.05 compared with block 1.

Figure 6.

Rats exhibit either high or low levels of impulsivity during the delay discounting task. HI, n = 3 males and 6 females; LI, n = 6 males and 3 females. There was no significant difference in sex distribution across groups (Fisher's exact test, p = 0.347). A, Percentage delay choice (large reward chosen) during free choice trials in HI versus LI rats. B, Accuracy (percentage correct responses) in HI rats on recording day. C, Accuracy (percentage correct responses) in LI rats on recording day. *p < 0.05 compared with block 1.

Figure 7.

Proportion of neurons exhibiting responsive cell firing during free choice cue presentations in HI (A) versus LI (B) rats across blocks and proportion of neurons exhibiting responsive cell firing during free choice lever presses in HI (C) versus LI (D) rats across blocks. *p < 0.05 compared with block 1, # p < 0.05 comparing HI and LI rats.

Figure 8.

Anatomical distribution of electrode tip placements in the PrL. Numbers indicate distance (mm) anterior to bregma.