We may take it for granted that the food we buy or grow is safe to eat, but for some species information passed between peers can help to indicate whether a new potential food source is safe or not. A team of neuroscientists at the University of Geneva (UNIGE) in Switzerland has now identified how social contact, sensory stimuli, and neural connections are linked to help instruct food choice in rodents. The studies, published in Science, also highlight the role of social connection in the interpretation of sensory stimuli, and in the animals’ ability to adapt to their environment.

“To understand how the brain perceives food, we looked at food choices in an animal model, and more specifically how these choices are being built and whether they can be influenced,” said Christian Lüscher, PhD, a professor in the department of basic neurosciences at UNIGE Faculty of Medicine. Lüscher and colleagues reported on their findings in a paper titled, “Social transmission of food safety depends on synaptic plasticity in the prefrontal cortex.”

Food consumption is ultimately driven by the body’s metabolic needs, but when we eat can be influenced by external factors, the authors wrote. The threat of a predator may stop a hungry animal from eating, while particularly tasty food may prompt overeating, leading to fat deposition. Animals can also use information derived from their neighbors to direct their food selection. Primates rely on predominately visual cues, the researchers continued, whereas rodents use their olfactory system to detect odors, including carbon disulfide, CS2, in other rodents’ breath. “Such social transmission of food preference (STFP) occurs when an observer mouse exposed to a demonstrator mouse fed with scented food drives a preference for that food over a differently scented alternative.”

Studies have started to unpick how olfactory sensory neurons relay information to specific brain regions, and Lüscher’s team has for years been investigating brain mechanisms linked to nutrition. For their latest studies, the team studied food choices in mice. Wild mice living in colonies of a few dozen animals can adapt to environments and find new food sources. To limit the risk of poisoning, designated “taster” mice assess the safety of unknown foods. “But then how do they pass on the information to their peers?” queried Michaël Loureiro, PhD, a researcher in Lüscher’s laboratory. “Can these few mice permanently change the feeding behavior of the whole group? We wanted to understand how, in the brain, the balance between the innate and the acquisition of new behavior through social contact is forged.”

Mice will naturally choose thyme flavor over cumin, but they can be trained to eat cumin-spiced food. To test how mice can transmit food choice and feeding behavior to their peers, the researchers put a “demonstrator” mouse that had eaten a cumin-flavored meal into contact with an “observer” mouse that still had a preference for thyme. The two mice were housed in the same cage for 30 minutes, and 24 hours later the observer mouse was presented with a choice of two meals, one flavored with thyme, the other with cumin. Having been housed the day before with the cumin-eating demonstrator, the observer mouse showed interest in cumin, indicating that it had detected the cumin odor molecules on the demonstrator mouse. Interestingly, this only worked if the food source was unfamiliar to the observer. “ … corroborating the transmission of a safety signal, rather than passing a mere preference.”

Detection of a specific odor and CS2 by the olfactory bulb activates neurons in the piriform cortex (PiC), which then triggers neuronal signaling. The researchers tagged neurons that played a role in transmitting and translating the olfactory information from demonstrator to observer, including neurons that project to the nuclear accumbens (NAc) projectors in the medial prefrontal cortex (mPFC), and the paraventricular nucleus of the thalamus (PVT), which are, respectively, involved in decision making and the expression of aversive memories. “We observed that not only did these neurons receive information from the olfactory sensory cortex, but also that inter-neural communication was modified as a result,” noted Loureiro. “Learning a new smell strengthens synaptic connections and modifies the animal’s natural choice after contact with its fellow mouse according to a specific brain path: first, the olfactory system detects the smell. The olfactory cortex then connects to the pre-frontal cortex, involved in decision-making choices, which in turn is connected to the ventral striatum, which manages motivation and the search for a reward.”

When the team used a technique known as optogenetics to switch off the neural changes induced when the two mice were in contact, the observer mouse exhibited no cumin memory. “And the mouse turned away from the cumin,” Lüscher stated. “By removing the reinforcement of connections in the network that we had identified, we proved that the mechanism we suspected was necessary for learning through social contact.”

The authors say their results confirm that signaling pathways targeting the NAc are essential for food preference driven by olfactory cues in a social context. “ … we demonstrate that STFP acquisition increases the excitatory transmission at PiC-to-NAc projectors in the mPFC, which is the cause of the altered behavior. Our study thus adds a circuit to the complexity of food intake behavior that may override immediate metabolic needs in the interest of survival.”

The UNIGE scientists’ results provide new insights into the neurobiological mechanisms of social interactions and associated learning. It’s feasible that disruption to or dysfunction of similar mechanisms in humans may underpin social difficulties in individuals with autism. If the sensory cortex is unable to handle external stimuli, peer information may not be integrated adequately into the prefrontal cortex, which will then disrupt further transmission, making it harder to interpret external stimuli. “Understanding what networks and mechanisms are needed to integrate new information received from another individual and how this information is then used to adapt to the environment are fundamental questions,” Loureiro noted. “Indeed, these mechanisms appear to be dysfunctional in some neurodevelopmental disorders, such as autism spectrum disorders.”

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