Rat behavior and dopamine release are modulated by conspecific distress

Abstract

Rats exhibit ‘empathy’ making them a model to understand the neural underpinnings of such behavior. We show data consistent with these findings, but also that behavior and dopamine (DA) release reflects subjective rather than objective evaluation of appetitive and aversive events that occur to another. We recorded DA release in two paradigms: one that involved cues predictive of unavoidable shock to the conspecific and another that allowed the rat to refrain from reward when there were harmful consequences to the conspecific. Behavior and DA reflected pro-social interactions in that DA suppression was reduced during cues that predicted shock in the presence of the conspecific and that DA release observed on self-avoidance trials was present when the conspecific was spared. However, DA also increased when the conspecific was shocked instead of the recording rat and DA release during conspecific avoidance trials was lower than when the rat avoided shock for itself.

Anterior Cingulate Cortex Signals Attention in a Social Paradigm that Manipulates Reward and Shock

“…It might be argued that the main reason why, here, ACC seems to encode social attention, but not vicarious emotion, is that rats performing the current task did not exhibit empathy. This is certainly possible, as we will discuss in the next paragraph, but it is important to point out that our rats did freeze, suppress food cup behavior, and approach when the other rat froze during shock-other trials, which other studies have used as evidence for empathy in rodents [16,36,37,40,42,44,[46][47][48]51]. Moreover, also consistent with previous work, we show that, when a rat is not experiencing shock, they exhibit less empathetic behavior [37,42,45,47].…”

“…First, let us consider blocks of trials where both the recording rat and the conspecific received outcomes (i.e., R/R trial blocks; Figure 2, top row). As shown previously, prior to outcome delivery, beam breaks increased and decreased on reward-self (blue) and shock-self (red) trials relative to neutral (orange) trials (Figure 2A), respectively [36]. After the presentation of the directional light cue (i.e., the cue that informed the rat which animal would receive the outcome), there was a significant increase in food cup entries for reward-self compared to reward-other trials, demonstrating that rats anticipated the receipt of reward before its delivery (Figure 2I, dark versus pale blue; Wilcoxon; z = 5.326; p < 0.001).…”

“…Although many studies have shown rats to exhibit empathetic and pro-social behaviors [15,37,38,39,42,[53][54][55], we have found that rats can be rather ''self-interested''. This has been evident in our studies examining dopamine (DA) release in nucleus accumbens in a version of the Pavlovian task described here [36,51]. For example, we have shown that rats emit appetitive vocalizations and DA is released during rewards delivered to conspecific but only early during learning.…”

“…After rats experienced several trials where the conspecific received reward and they did not, vocalizations became aversive and DA was inhibited during conspecific reward delivery [51,56,57]. Further, we have shown that DA is released when the recording rat observes the conspecific receive shocks, suggesting that observation of the conspecific receiving shock, instead receiving shock itself, is an event that is better in value than expected [36]. Therefore, in tasks where rats are selfinterested-such as in an appetitively/aversively competitive context-and circumstances are well learned, ACC may contribute more to social attention.…”

“…was administered twice daily for two weeks post-operatively to prevent infection. REAGENT In the reported experiments we utilize a modified version of a task previously published [36], described in detail below. Recordings were collected in a modified shuttle box chamber (Figure 1A; 16 in x 6.25in x 8.375 in; WDH; Med Associates; n = 6 rats).…”