Towards a unified theory of emotional contagion in rodents—A meta-analysis. Julen Hernandez-Lallement, Paula Gómez-Sotres, Maria Carrillo. Neuroscience & Biobehavioral Reviews, October 3 2020. https://doi.org/10.1016/j.neubiorev.2020.09.010
Highlights
• Rats and mice show comparable levels of emotional contagion, however, only mice strain-specific differences in emotional contagion response.
• Rats and mice show an equivalent contagion response to familiar and unfamiliar conspecifics.
• Prior experience with an emotional inducing stimulus significantly increases fear contagion response in rats but not in mice.
• Social testing condition influences the level of contagion: animals tested alone show reduced contagion compared to animals tested in a group.
Abstract: Here we leverage 80 years of emotional contagion research in rodents and perform the first meta-analysis on this topic. Using 457 effect sizes, we show that, while both rats and mice are capable of emotional contagion, there are differences in how various factors modulate empathy in these species: 1) only mice show strain-specific differences in emotional contagion response; 2) although rats and mice have equivalent contagion response to familiar and unfamiliar individuals, our results show that familiarity length is negatively correlated with level of contagion in rats only; 3) prior experience with emotional stimuli almost doubles fear contagion response in rats while no changes are detected in pre-exposed mice; 4) both mice and rats tested alone show comparable reduced contagion compared to animals tested in a group; 5) emotional contagion is reduced in animals from both species missing one sensory modality compared to situations where all sensory modalities are recruited during emotional contagion. Lastly, we report similar patterns of brain activation during emotional contagion in rats and mice.
Keywords: Emotional contagionMeta-analysisRodentsEmpathy
4. Conclusion and limitations
4.1. Updating current models of emotional contagion
While a high number of reviews attempting to summarize the literature on emotional contagion in rodents were published in recent years (Keysers and Gazzola, 2016; Meyza et al., 2016; Keum and Shin, 2016; Sivaselvachandran et al., 2016; Mogil, 2012; Lukas and de Jong, 2016; Keum and Shin, 2019), one article in particular went one step further and proposed a classification of experimental approaches used in the field (Panksepp and Panksepp, 2013a). This classification distinguished a variety of phenomenon such as contagion, social analgesia, social buffering, social priming, behavioral matching and social transfer. In the current meta-analysis, we updated and simplified this classification based on our revised inclusion criteria for studies measuring emotional contagion: ‘a study measuring a behavioral response associated with (indirectly -in absence of- and directly -in presence of others-) the emotional cues of other individuals’. This means that all the phenomena mentioned above, per our definition, fall under the emotional contagion umbrella. One illustrative example is the case of social buffering, where a distressed animal shows reduced fear when paired with a neutral non-distressed conspecific. In these cases, we considered the observed phenomenon as emotional contagion from an animal in a neutral emotional state to one in a fearful state. This approach allowed us to unify different paradigms, and seemingly diverse approaches on rodent empathy into a single model. Our classification had additional key differences with the classification proposed by Panskepp & Panksepp (Panksepp and Panksepp, 2013a): 1) contagion can occur without the direct presence of an individual (e.g., through a cotton boll soaked with urine of a fearful animal); 2) emotional contagion paradigms consist of three phases: pre-exposure, emotional transfer and measure of emotional contagion; 3) the term emotional transfer refers to the point in time in which the emotional state from one individual is contaged to another (measurement time could happen during or after emotional transfer); 4) measurements of emotional contagion had to recruit an emotional observable response; if they failed to do so (such as memory effects), they were not considered direct measurements of emotional contagion but rather secondary processes related to emotional contagion. All the studies included in the current meta-analysis fall under this classification.
4.2. Limitations
While we strived to reduce the number of arbitrary decisions that needed to be made (by devising a clear methodology and procedures in the decision process), inevitably, we did encounter difficult choices at different stages of the process. In particular, for each study, we were confronted with interpreting whether the reported data was a direct measure of emotional contagion, or rather a secondary process triggered by emotional contagion. The lack of clear definitions and unity in the field made it challenging in deciding which data was indeed relevant for this meta-analysis. In order to guide our decisions, we elaborated a framework through which each study was pipelined to take a decision on whether the effect size reflected emotional contagion-related data. For instance, research performed on social transmission of taste aversion can be arguably included in the emotional contagion field, since, typically in these paradigms, one animal undergoes an aversive emotion (taste), which is thereafter transmitted to a naïve conspecific through interactions. However, these publications were not included in this meta-analysis due to the fact that the aversive emotion experienced by the demonstrator was often not measured and quantified, nor was the actual transfer of emotion. Similar issues were encountered in studies where emotional contagion was used as a tool, rather than a measure, to study how observing the distress of others affected cognitive abilities later in time, such as memory and learning (Nowak et al., 2013; Ito et al., 2015a). Albeit these are important effects of emotional contagion in other neural processes and behaviors, they are not a direct measurement of emotional contagion, and as such were excluded from the main analysis.
However, we find it important to emphasize the caveats of our approach by pointing out other missing aspects of the emotional contagion literature. For instance, the filters used in this study failed to capture articles on mother-pup interaction and the emotional transfer inherent to such social systems (Moriceau and Sullivan, 2006; Barr et al., 2009). Future meta-analytic work on this topic could increase their search filter range to include such studies and encompass even more variability in rodent emotional contagion.
It should also be noted that our filters might have failed to include articles where similar processes were studied but other wording was used. It is notable that rodent emotional contagion is a controversial topic (Balter, 2011) and several studies have framed their results in terms of stress-related processes instead of emotional contagion (Breitfeld et al., 2015; Zalaquett and Thiessen, 1991; Mackay-Sim and Laing, 1981). While we believe that the high number of effect sizes and studies included in this meta-analysis already allow for careful conclusions to be drawn, future endeavors should carefully increase the granularity of their filters to encompass studies that investigated similar processes under a different framework.
Another limitation of our work is the low number of effect sizes present in some distributions. For instance, the low number of effect sizes reported in females makes it difficult to conclude on the results reported here, that is, that sex does not modulate emotional contagion. Similar parsimony should be used when interpreting effect sizes reported in different strains. For instance, the differences reported between CD-1 and CF-1 mice, two very close strains, are quite surprising. One likely explanation for this (and other) differences might lie in the experimental paradigm used, which differed between strains. These discrepant results suggest that additional, more granular variables should be added to future meta-analysis. For instance, an attempt at classifying experimental paradigms to identify contexts and situations where emotional contagion might be more salient would allow to associate differences in effect sizes to experimental manipulations rather than to species, strains or other parameters.
This meta-analysis revealed that, although, emotional contagion can occur in response to both positive and negative emotions, as already noted by (Panksepp and Panksepp, 2013c), to date nearly all studies investigating emotional contagion in rodents use negative stimuli to trigger emotional transfer, which could be due to the fact that in rodent empathy research negative reinforcers are traditionally used. This observation stresses the need to use positive reinforcers to study the other side of rodent empathy, as already performed in some studies (Willuhn et al., 2014b; Kashtelyan et al., 2014b; Lichtenberg et al., 2018), and more generally in the field of prosocial behavior (Lichtenberg et al., 2018; Márquez et al., 2015; Hernandez-Lallement et al., 2016b, 2020). A promising avenue would lie in studies that directly compare the effects of positive and negative reinforcers, although we acknowledge that developing comparable positive and negative stimulus is a challenge given the higher saliency and reinforcing power of negative stimuli. On the other hand, it is important to consider the possibility, that the under reporting of studies using positive stimuli could be due to lack of effect of this type of stimuli and bias to report null effects.
A final limitation that we encountered was the incomplete reporting of information, namely, the methods section. We noticed that some variables more likely to not be properly reported such as age and number of days that observers and demonstrators were related to each other, with 13 % and 21 % of overall missing values per category respectively. In addition, our quantitative analysis suggested that randomization, blinding and sample size calculations are seldom reported (and/or done) in studies in the field, which overall reduces the results quality.
4.3. Conclusion
Overall, this is the first meta-analysis and systematic review conducted to date on the field of rodent emotional contagion. In this meta-analysis we develop an umbrella definition of emotional contagion that covers a large rage of studies investigating this response. We also developed a classification model that allowed us to unify a range of existing paradigms used to investigate emotional contagion. Within this model we identified key parameters that have a modulatory effect on emotional contagion and that can be used for optimizing the design of future studies in the field. However, we underscore that many differences reported here should be taken cautiously since the lack of effect sizes and major differences in experimental paradigms could still account for effects we report in this meta-analysis. We also identify a range of brain regions that can be used as targets for further to further our understanding of the neural mechanisms of emotional contagion. Lastly, this meta-analysis also identifies gaps in knowledge and potential research areas of interest.
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