Results are therefore inconsistent with claims in the literature that rats are altruistically motivated to share food with other rats, even when food is abundant

Failure to Find Altruistic Food Sharing in Rats. Haoran Wan, Cyrus Kirkman, Greg Jensen and Timothy D. Hackenberg. Front. Psychol., June 22 2021. https://doi.org/10.3389/fpsyg.2021.696025

Abstract: Prior research has found that one rat will release a second rat from a restraint in the presence of food, thereby allowing that second rat access to food. Such behavior, clearly beneficial to the second rat and costly to the first, has been interpreted as altruistic. Because clear demonstrations of altruism in rats are rare, such findings deserve a careful look. The present study aimed to replicate this finding, but with more systematic methods to examine whether, and under what conditions, a rat might share food with its cagemate partner. Rats were given repeated choices between high-valued food (sucrose pellets) and 30-s social access to a familiar rat, with the (a) food size (number of food pellets per response), and (b) food motivation (extra-session access to food) varied across conditions. Rats responded consistently for both food and social interaction, but at different levels and with different sensitivity to the food-access manipulations. Food production and consumption was high when food motivation was also high (food restriction) but substantially lower when food motivation was low (unlimited food access). Social release occurred at moderate levels, unaffected by the food-based manipulations. When food was abundant and food motivation low, the rats chose food and social options about equally often, but sharing (food left unconsumed prior to social release) occurred at low levels across sessions and conditions. Even under conditions of low food motivation, sharing occurred on only 1% of the sharing opportunities. The results are therefore inconsistent with claims in the literature that rats are altruistically motivated to share food with other rats.

Discussion

The present experiment was designed to replicate and extend some key conditions described by Ben-Ami Bartal et al. (2011), in which rats chose between social release and food. The present research focused on two main findings from that study and their related conclusions: (1) rats chose food and social release with similar latencies, and therefore, food and social release are equally valued; and (2) rats willingly share food with their social partner, even if it comes at a cost to the individual. Taken together, these findings provide key support for the authors' claims of altruistic food sharing. Because occurrences of such unreciprocated food sharing are rare in the published literature (Clutton-Brock, 2009; Taborsky et al., 2016), they warrant further scrutiny.

With respect to the first claim of equal reward value of social release and food, we found that relative value of food and social release varied systematically across conditions. More specifically, when food motivation was low (i.e., the focal rat had unrestricted homecage access to chow in their home cage) and food quantity was high (4–5 pellets per trial), food and social release were chosen about equally often (Conditions 4, 6, and 7), consistent with the (Ben-Ami Bartal et al., 2011) findings. When food motivation was high (restricted access to food outside the session), however, rats clearly preferred food over social release (Conditions 1–3). This finding is consistent with the Hiura et al. (2018) findings, showing strong and reliable preference for food over social release when food is restricted outside the session (see also Blystad et al., 2019). Taken as a whole, the presents results show that relative preference between social and food is not invariant, but rather, is subject to reward and motivational variables (food quantity and overall food access). The relative value of social release and food are always subject to these (and other) variables, and it would therefore be premature to draw broad conclusions about their relative value from sampling only a limited range of conditions. In any case, a motivational view of social and food rewards helps explain discrepant findings from prior research.

The changes in preference across manipulation of food quantity in the first three conditions were driven mainly by changes in the number of food choices per session. This is partly due to economic factors (i.e., decreasing unit price of food) and partly due to satiation. Given the low price (1 response) and the dozens of choice opportunities each session, rats produced and consumed large numbers of sucrose pellets each session when chow in their home cage was restricted (37–284 pellets, mean = 131 across rats). By contrast, when home cage chow was unlimited and food motivation was low, subjects consumed substantially fewer pellets (16–107 pellets, mean = 66 across rats). And when coupled with unlimited food access outside the session in Condition 4, the procedures combined to produce conditions of low food need. Indeed, our rats had such an abundance of food, there was often food left at the end of the food collection periods of Conditions 5–7 (up to 26% of all pellets in Condition 5), even if there was no restrained rat with which to share them. That rats did not consume rewards as highly valued as sucrose pellets suggests a high degree of satiation.

Despite such low levels of food need, there was very little evidence of food sharing – the second and more controversial claim set forth by Ben-Ami Bartal et al. (2011). Behavior that met our operational definition of sharing (i.e., producing food and then releasing the rat while food remained available) was infrequent across all conditions in the experiment, with zero shared pellets being the most common outcome across sessions and the mean being about 1 pellet per session. It did not matter whether food access outside the session was restricted (Conditions 1–3) or not (Conditions 4–7); nor did it matter how many pellets were produced per response (Condition 1–3): rats rarely shared with the other rat any of the abundant supply of food pellets they produced each session. Even in the final two conditions, with procedures that most closely matched the original study (i.e., symmetrically arranged social and food locations, 5 sucrose pellets, and unrestricted access to food and social contact outside the session), sharing was seldom observed (see also Supplementary Video 1). Thus, on the whole, we found no evidence to support the 2011 claim by Ben-Ami Bartal et al. that a rat willingly shares food with another rat.

There is no simple way to reconcile the food sharing reported by Ben-Ami Bartal et al. (2011) with the near complete absence of sharing in the present study. Low levels of food sharing cannot be explained in terms of reduced opportunities for sharing, as the number of social releases (hence, sharing opportunities) remained fairly constant across conditions for individual rats (see Figures 3, 6). This was accomplished by providing repeated exposure to a consistent duration of social contact (30 s) across the experiment. With long sessions and repeated trials, rats had ample opportunities to share the food they had produced; they simply did not do so. The discrepant results also cannot be explained in terms of differing definitions of sharing between experiments. Ben-Ami Bartal et al. (2011) used a less stringent indirect measure of sharing (difference between food consumed with and without a rat available to release) than our behavioral definition of sharing (produce food, then social release with food remaining). This alone cannot be responsible for the different results, however, for even if we adopt the less stringent criterion, our rats showed no differences in food consumption with or without a rat available to release (Figure 7). This is important, as evidence of sharing-related costs are crucial to an altruistic food sharing explanation. Thus, by neither definition did our rats engage in sharing.

We recognize that the present study relies on a small sample size of three rats. Even so, the evidence against food sharing is strong. Across all of the conditions in which sharing was possible, our rats earned an average of 2,171 rewards each (1,662 to 2,772 across rats) of which they shared an average of 47 (0 to 85, across rats), or 1% of the total rewards earned. Because each earned reward provided a sharing opportunity, our rats had vastly greater food sharing opportunities than rats in the Ben-Ami Bartal et al. (2011) experiment. Precise estimates of food sharing opportunities in that experiment are difficult, both because opportunity per reward cannot be derived from the data presented in the paper (% trials with sharing), and because it took the rats several sessions to learn to open the door for either option (before which rewards were not actually available to share). Nonetheless, the theoretical maximum would be 60 food sharing opportunities (five rewards per trial for 12 trials) per rat, roughly 1% of the number food-sharing opportunities in the present study. In addition to vast opportunities for food sharing, the present procedures produced consistent patterns of preferences across animals and over consecutive sessions. Thus, while the small number of rats in the present study limits our ability to generalize to the population of all rats, we have considerable confidence in the results with these particular rats: all were strongly disinclined to share food with their partners across all conditions and thousands of sharing opportunities. Perhaps only some rats engage in altruistic food sharing, differing from their non-sharing conspecifics for some reasons yet to be discovered, and that our sample happened to include only selfish rats who happen to be selfish in very similar ways. This seems unlikely, but it will nevertheless be important to replicate with larger samples of rats in future research.

Another difference between the studies is the food itself. Ben-Ami Bartal and colleagues used a single presentation of 5 chocolate chips, which amounts to approximately 12 calories of food, contained in about 1.62 g. By comparison, each of our sucrose pellets constitutes approximately 0.17 calories, each with a mass of 0.045 g. When subjects had unlimited home cage access to chow, they therefore tended to consume about 11.2 calories of food. Furthermore, rats in Condition 5 (with no opportunity for social access) left about 6 pellets (worth about 1 calorie) behind, despite having no external motivation to do so. This points to subjects with free access to chow leaving high-quality food unconsumed due to satiation, usually doing so shy of 12 calories. If rats with low food motivation are inclined to leave food unconsumed relatively frequently in the absence of conspecifics, it is difficult to argue that losing such food due to sharing can be understood as a “cost.” Ben-Ami Bartal and colleagues give no rationale for their choice of 5 chocolate chips, but based on the patterns of non-social food intake observed in the present study, it seems likely that, had they used 3 chocolate chips, that would have observed almost no sharing, whereas if they had used 7 chocolate chips, they would have observed relatively frequent sharing.

There are other differences between the procedures, and the only way to know for certain which factors are responsible for the discrepant results would be to begin with a direct replication, an exact reproduction of the original procedures, and thereafter change one variable at a time. We chose instead to conduct a systematic replication (Sidman, 1960), in which some, but not all, of the original procedures are reproduced. Systematic replications are useful in assessing the generality of a finding, and this fit with our broader objectives of providing a more thorough characterization of preference and sharing. We sought not only to replicate but to extend, to assess the generality of the findings by exploring behavior across a range of conditions, including but not limited to, those of the original study. In particular, the lack of adequate control conditions leaves the original study open to multiple interpretations. Sampling independent variables under varying conditions puts replication efforts into a broader context, changing the focus from binary questions with yes-no answers (e.g., Do rats value social release over food? Do rats share food with another rat?) toward conditional questions (e.g., Under what conditions is social release favored over food, and vice versa? Under what conditions does sharing occur?). Viewed in this way, Ben-Ami Bartal and collaborators are not so much incorrect as they are interpreting incomplete evidence; their results are part of more general relationships between preference and sharing and the variables of which they are a function.

Exploring such functional relationships across a parametric range can also shed light on theoretical disputes. For example, when examined at only a single point on a function, social release can be interpreted either in terms of social reward (response-contingent access to social interaction) or in terms of empathy (acting out of concern for the other rat): both accounts make the same prediction that door opening will occur. The accounts begin to differ, however, as behavior is examined while other experimental parameters change. For example, in procedures similar to those used here, Vanderhooft et al. (2019) first trained social release in rats, then systematically increased the price of social release (number of responses to produce it) across sessions, generating demand functions. Overall, the functions (27 in all) were well-described by the Hursh and Silberberg (2008) essential value model, a model that has proven useful in quantifying the value of numerous other rewards, including food, water, and drugs (Hursh and Roma, 2016). In other words, rates of social release behavior were predictable, with a high degree of quantitative precision, on the basis of these social reward functions. It is less clear, however, what, if anything, an empathy account would have to say about these data: it makes no obvious predictions about how empathy is affected by price – or other variables known to affect reward value (e.g., magnitude, delay, or probability), about which social reward makes clear and testable predictions. And if predictions could be derived from an empathy account (e.g., by assuming that empathy mirrors social reward functions), they would be indistinguishable from the more parsimonious social reward account, and would therefore add little to the explanation. This is not to deny the importance of empathy as a topic worthy of scientific study; it is, rather, to demand more stringent tests of it, especially in domains in which simpler explanations already exist.