Social transmission of food safety depends on synaptic plasticity in the prefrontal cortex

Abstract

When an animal is facing unfamiliar food, its odor, together with semiochemicals emanating from a conspecific, can constitute a safety message and authorize intake. The piriform cortex (PiC) codes olfactory information, and the inactivation of neurons in the nucleus accumbens (NAc) can acutely trigger consumption. However, the neural circuit and cellular substrate of transition of olfactory perception into value-based actions remain elusive. We detected enhanced activity after social transmission between two mice in neurons of the medial prefrontal cortex (mPFC) that target the NAc and receive projections from the PiC. Exposure to a conspecific potentiated the excitatory postsynaptic currents in NAc projectors, whereas blocking transmission from PiC to mPFC prevented social transmission. Thus, synaptic plasticity in the mPFC is a cellular substrate of social transmission of food safety.

Role of Projections between Piriform Cortex and Orbitofrontal Cortex in Relapse to Fentanyl Seeking after Palatable Food Choice-Induced Voluntary Abstinence

“…Ross and Eichenbaum (2006) reported that memory retrieval of social transmission of food preference is associated with increased Fos expression in the Pir (and OFC). Loureiro et al (2019) showed a critical role of a Pir to prefrontal cortex projections in this behavior. Acquisition of conditioned flavor preference is associated with increased Fos expression in the Pir (Mediavilla et al, 2016), and lesions or antagonists of NMDA or cannabinoid type 1 receptors decrease conditioned flavor preference (Mediavilla et al, 2016;Mukherjee and Yuan, 2016;Terral et al, 2019).…”

The Grueneberg ganglion controls odor-driven food choices in mice under threat

“…Especially, when confronted to food scarceness, behavioral tradeoffs need to be made 2,3 . Olfactory senses play an important role in this process as they help to find food but also to sense and avoid threatening situations [4][5][6][7][8][9] such as predation. For rodents, the attraction to food is primarily determined by familiarity, as scents of known food are innately favored 2,10 .…”

“…These scents are detected by olfactory sensory neurons (OSNs) found in the main olfactory epithelium (MOE) 11,12 . Food familiarity can be acquired via communication between individuals, by the so-called "social transmission of food preference" (STFP), a behavioral process that occurs by sniffing the breath of conspecifics and making an association between the novel food scent and the presence of the endogenously produced carbon disulfide gas (CS 2 ) 4,13,14 . For this process to occur, the concomitant recognition of the food odorant by OSNs and the detection of the CS 2 by guanylyl cyclase-D neurons (GC-D) of the MOE is essential.…”

Ventral midline thalamus is not necessary for systemic consolidation of a social memory in the rat

“…*p < 0.05 versus innate cumin preference. Ross et al, 2005) and damage or dysfunction at any level in this circuit seems to have disruptive consequences on STFP acquisition or recall (Brightwell et al, 2005;Bunsey and Eichenbaum, 1995;Jeon et al, 2007;Loureiro et al, 2019;Peters et al, 2003;Ross and Eichenbaum, 2006;Ross et al, 2005). Therefore, information exchange between cortical and hippocampal modules underlying systemic consolidation could occur in this circuitry, which does not require the ReRh nuclei hub.…”

“…Lesburguères et al (2011) also showed that upon information encoding, OFC neurons undergo a tagging process, which might serve as a matrix for hippocampus-driven cortical rewiring supporting enduring memory. Recently, Loureiro et al (2019) found STFP to depend on projections from the piriform cortex—one of the olfactory projection areas to which the study by Ross and Eichenbaum had pointed—to the neurons of the mPFC (prelimbic and infralimbic regions), which project onto the nucleus accumbens. Thus, STFP seems to involve several distributed and interdependent structures of the brain.…”