Environmental luminance impairs socio-sexual recognition memory through a succinct retina to supraoptic nucleus circuit

Abstract

Social memory between the same gender or even different gender is a complex and heavily modulated process in the nervous system. It is important for an individual to form social memory between the opposite sex to either increase mating opportunities with multiple partners or form monogamous pair bonding. Therefore, a specific neuronal circuit to regulate social sexual memory may enhance the mating opportunity for an individual. It has been shown that both the auditory and somatosensory systems could increase the activity of oxytocin neurons in the paraventricular nucleus to regulate social behaviors. Although light exposure could influence various forms of memory, such as fear and object memory, how luminance signals modulate social recognition memory remains unclear. Here, we show that acute light exposure could impair the socio-sexual recognition memory (SSRM) in male mice. Contrary to sound and touch, light stimulation could inhibit oxytocin neurons in the SON (SONOT) through M1 SON-projecting ipRGCs and GABAergic neurons in the peri-SON (pSONGABA). Optogenetic activation of SONOT neurons with channelrhodopsin is sufficient to enhance the SSRM performance in male mice, even under light conditions. Our results show that the visual system could modulate SSRM through a succinct ipRGCs-pSONGABA-SONOT neuronal circuitry. Together, we demonstrate a dedicated neuronal circuit of how luminance affects memory formation for an individual toward different sex through the oxytocin system, a powerful modulatory neurohormone in the central nervous system.