Social Transmission and Buffering of Hippocampal Metaplasticity after Stress in Mice

Abstract

In social animals, the behavioral and hormonal responses to stress can be transmitted from one individual to another through a social transmission process, and, conversely, social support ameliorates stress responses, a phenomenon referred to as social buffering. Metaplasticity represents activity-dependent synaptic changes that modulate the ability to elicit subsequent synaptic plasticity. Authentic stress can induce hippocampal metaplasticity, but whether transmitted stress has the same ability remains unknown. Here, using an acute restraint-tailshock stress paradigm, we report that both authentic and transmitted stress in adult male mice trigger metaplastic facilitation of long-term depression (LTD) induction at hippocampal CA1 synapses. Using LTD as a readout of persistent synaptic consequences of stress, our findings demonstrate that, in a malemale dyad, stress transmission happens in nearly half of naive partners and stress buffering occurs in approximately half of male stressed mice that closely interact with naive partners. By using a social-confrontation tube test to assess the dominantsubordinate relationship in a male-male dyad, we found that stressed subordinate mice are not buffered by naive dominant partners and that stress transmission is exhibited in ;60% of dominant naive partners. Furthermore, the appearance of stress transmission correlates with more time spent in sniffing the anogenital area of stressed mice, and the appearance of stress buffering correlates with more time engaged in allogrooming from naive partners. Chemical ablation of the olfactory epithelium with dichlobenil or physical separation between social contacts diminishes stress transmission. Together, our data demonstrate that transmitted stress can elicit metaplastic facilitation of LTD induction as authentic stress.

Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model

“…Long-term depression is another kind of synaptic plasticity, which is enduring changes in synaptic strength, as a cellular model of information storage and process in the CNS ( Martin et al, 2000 ), and which is used to assess the stress in adult male mice ( Lee et al, 2021 ). In our work, we found a weaker cortical LTD in the superficial and deep layers of the aIC in observer and demonstrator mice, but there was no significant difference between them.…”

Emotional contagion and prosocial behavior in rodents

“…(Figure 4B), in which an observer can freely interact with a demonstrator that has been stressed (e.g., previously restrained, defeated, shocked, acid or bee venom injected, or presented with a CS+), the observer not only approaches but also sniffs, licks, touches, and allogrooms the stressed demonstrator and does so more often and for longer than when interacting with a nonstressed conspecific [27,49,66,[114][115][116][117][118][119]. The stressed demonstrator, in contrast, engages more in nonsocial behaviors such as self-grooming, digging, rearing, and nesting [115,118,119]. Stressing the observer itself reduces its proximity seeking [12,[120][121][122] (but see [49]).…”

“…The motive to approach and interact with distressed demonstrators remains somewhat unclear, but such curiosity could have two benefits. Firstly, proximity maximizes the observer's access to the alarm pheromones produced by the demonstrator, which are most effective at close range [123] and trigger physiological and behavioral changes in approachers when direct contact is possible [96,118,124]. The resulting increase in pheromone exposure increases emotional contagion, including changes in pain sensitivity [27,49] and neural plasticity [118,124], thereby increasing the observer's preparedness to deal with similar threats.…”

“…Firstly, proximity maximizes the observer's access to the alarm pheromones produced by the demonstrator, which are most effective at close range [123] and trigger physiological and behavioral changes in approachers when direct contact is possible [96,118,124]. The resulting increase in pheromone exposure increases emotional contagion, including changes in pain sensitivity [27,49] and neural plasticity [118,124], thereby increasing the observer's preparedness to deal with similar threats. Proximity seeking can thus be conceived of as a social form of risk assessment that benefits the approaching observer: a propensity that leads to the collection of valuable information about potential dangers [108].…”

“…Indeed, also for pups, fear is best transferred from mothers if the mother engages in direct contact with her pups [125]. Secondly, the proximity of, and allogrooming by, the calmer observer provides the demonstrator with calming pheromones [96] and leads to social buffering [24,[114][115][116]118,119,124,126,127]. Proximity seeking can thus also be conceived of as a form of consolation that benefits the approached demonstrator [5,12,49,66,[114][115][116]120,121,128].…”