Long-Term Social Recognition Memory Is Mediated by Oxytocin-Dependent Synaptic Plasticity in the Medial Amygdala

• Published in: Biological psychiatry (1969) 2014-09, Vol.76 (5), p.377-386
• Main Authors: Gur, Rotem, Tendler, Alex, Wagner, Shlomo
• Format: Article
• Language: English
• Subjects: Amygdala - drug effects; Amygdala - physiology; Animals; Anisomycin - pharmacology; Biological and medical sciences; Discrimination (Psychology) - physiology; Long-term depression; long-term memory; Long-Term Synaptic Depression - physiology; Male; medial amygdala; Medical sciences; Memory, Long-Term - physiology; Memory, Short-Term - physiology; Neuropsychological Tests; Olfactory Bulb - physiology; oxytocin; Oxytocin - metabolism; Protein Synthesis Inhibitors - pharmacology; Psychiatry; Psychology. Psychoanalysis. Psychiatry; Psychopathology. Psychiatry; Rats, Sprague-Dawley; Receptors, Oxytocin - antagonists & inhibitors; Receptors, Oxytocin - metabolism; Recognition (Psychology) - physiology; Social Isolation; Social Perception; social recognition; synaptic plasticity
• ISSN: 0006-3223; 1873-2402
• DOI: 10.1016/j.biopsych.2014.03.022

Background Recognition of specific individuals is fundamental to mammalian social behavior and is mediated in most mammals by the main and accessory olfactory systems. Both these systems innervate the medial amygdala (MeA), where activity of the neuropeptide oxytocin is thought to mediate social recognition memory (SRM). The specific contribution of the MeA to SRM formation and the specific actions of oxytocin in the MeA are unknown. Methods We used the social discrimination test to evaluate short-term and long-term SRM in adult Sprague-Dawley male rats ( n = 38). The role of protein synthesis in the MeA was investigated by local application of the protein synthesis blocker anisomycin ( n = 11). Synaptic plasticity was assessed in vivo by recording the MeA evoked field potential responses to stimulation of the main ( n = 21) and accessory ( n = 56) olfactory bulbs before and after theta burst stimulation. Intracerebroventricular administration of saline, oxytocin, or oxytocin receptor antagonist was used to measure the effect of oxytocin on synaptic plasticity. Results Anisomycin application to the MeA prevented the formation of long-term SRM. In addition, the responses of MeA neurons underwent long-term depression (LTD) after theta burst stimulation of the accessory olfactory bulb, but not the main accessory bulb, in an oxytocin-dependent manner. No LTD was found in socially isolated rats, which are known to lack long-term SRM. Finally, accessory olfactory bulb stimulation before SRM acquisition blocked long-term SRM, supporting the involvement of LTD in the MeA in formation of long-term SRM. Conclusions Our results indicate that long-term SRM in rats involves protein synthesis and oxytocin-dependent LTD in the MeA.