How the hippocampus boosts your empathic sensitivity: A facilitator of vicarious emotions

Reference: Terranova, J. I., Yokose, J., Osanai, H., Marks, W. D., Yamamoto, J., Ogawa, S. K., & Kitamura, T. (2022). Hippocampal-amygdala memory circuits govern experience-dependent observational fear. Neuron, 110(8), 1416-1431.e13.

Do you remember the last time you saw something that really scared you? Maybe you were watching a horror movie? Maybe you witnessed a tragic accident or a crime? For most of us, the simple act of witnessing fear in others triggers strong emotional reactions. This phenomenon is known as emotional contagion: the process whereby observing emotions in others causes us to feel those emotions vicariously within ourselves. This automatic process is a fundamental component of empathic processing, which is essential for understanding others and daily social functioning. Observational fear is one example of emotional contagion, allowing us to vicariously experience the fears of another. But how do emotional experiences of fear get transferred from one person to another, even when they are not in danger themselves? Why is it that when watching a scary movie, we share feelings of fear with characters we observe?

What do we know about the neural underpinnings of observational fear?

Emotional contagion studies in rodents are frequently used to study observational fear and increase our understanding of empathy and prosocial behaviours. These experiments usually involve pairs of rats or mice, one labelled as the ‘observer’ and the other, the ‘demonstrator’. The demonstrator receives a foot-shock, triggering fear responses such as freezing. The observer witnesses the demonstrator during the delivery of foot-shocks, and although it does not receive a shock itself, the observer also displays freezing behaviour due to emotional contagion.

Typical emotional contagion paradigm where a demonstrator receives foot-shocks in the presence of an observer. Fear responses in the demonstrator are seen to be transferred to the observing animal by observational fear. From Han et al., 2019.

From previous emotional contagion experiments we know that several brain regions are involved in observational fear, including the anterior cingulate cortex (ACC) and basolateral amygdala (BLA). The ACC is an important region for emotional processing, mediating physical reactions to our emotional states1, while the BLA is typically associated with fear conditioning2. Previous studies highlighting key roles of ACC and BLA in the neural mechanisms of observational fear are plentiful. However, the limitations of such studies are that they often aim to elicit strong fear responses by giving frequent, strong shocks to the demonstrator to ensure observers will also show measurable changes in their behaviour. However, in real life, fear can often be expressed much more subtly whilst remaining recognisable. In other words, although we understand observational fear to be governed largely through ACC and BLA when demonstrators freeze substantially, we do not know whether the same mechanisms mediate observational fear when the demonstrator’s fear is less obvious to the observer.

Terranova and colleagues suggest that memories of prior experiences facilitate observational fear, particularly when there is a weak response from the demonstrator. The researchers hypothesised that given prior experience, previously unidentified, experience-dependent mechanisms within the brain allow us to interpret fear in others when behavioural changes are more subtle. To test their hypothesis, the researchers implemented a weaker shock protocol by halving both the number and intensity of shocks to the demonstrator.

Memory of prior experience influences the strength of observational fear

Previous research has shown that the hippocampus (HPC) is an important brain region mediating memory formation and recall; however, its role in observational fear remains unclear. Terranova and colleagues therefore wanted to examine a potential role for the HPC in experience-dependent observational fear. They found that projections from the HPC to the BLA seem to mediate observational fear behaviours in mice, through generation of memory engrams. Memory engrams are specialised groups of neurons, generated when these cells undergo chemical and/or physical changes during the process of new memory formation3. In this new research, the authors discovered a profound influence of two HPC regions in experience-dependent observational fear, mediated by the generation and reactivation of memory engrams in the BLA. First, they show that neuronal projections from the dorsal HPC to the BLA generate memory engrams in BLA during first-hand experiences of fear in the observer. Then, when witnessing fear in a demonstrator upon delivery of weak shocks, BLA engrams in the observer are reactivated by projections from the ventral HPC, allowing for the recognition of similar states of fear given subtle behavioural cues.

dHPC-BLA pathway mediates generation of memory engrams during first-hand experiences of pain (left). vHPC-BLA pathway mediates reactivation of engrams during fear observation, facilitating vicarious fear experiences (right). ACC-BLA pathway mediates observational fear, independent of memory. Adapted from Terranova et al., 2022.

What does this research teach us about the empathic brain?

Contrary to the expectations of the authors, this novel, experience-dependent pathway for observational fear processing does not involve the ACC. Rather, it seems that the ACC-BLA pathway is essential for observational fear when observed behaviours strongly reflect the emotional state of the observed individual. This pathway is independent of experience, allowing us to empathise with others without having had similar experiences ourselves. However, alongside the ACC-BLA pathway, parallel pathways from the HPC, discovered here by Terranova and colleagues, facilitate observational fear in the absence of strong behavioural cues by utilising memories of past experiences. These parallel pathways can be combined to elicit an even stronger observational fear response.

In this research, Terranova and colleagues provide a novel neural mechanism for how memory influences empathic processing within the brain. They show that our brains can actively draw upon memories of our own experiences when observing similar states in others, facilitating emotional contagion and vicarious experiences. It may be that this mechanism enhances our empathic sensitivity, such that we can understand others’ emotions even when their behaviours are quite ambiguous. Perhaps you will notice this the next time you watch a scary movie with friends – are you easily spooked? Or is your hippocampus triggering memories of your own experiences?

Additional References

1. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences4(6), 215-222.

2. Gale, G. D., Anagnostaras, S. G., Godsil, B. P., Mitchell, S., Nozawa, T., Sage, J. R., … & Fanselow, M. S. (2004). Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. Journal of Neuroscience24(15), 3810-3815.

3. Josselyn, S. A., & Tonegawa, S. (2020). Memory engrams: Recalling the past and imagining the future. Science367(6473), eaaw4325.