ReviewOxytocin, vasopressin, and social recognition in mammals
Introduction
The ability to recognize a familiar conspecific is the foundation for all mammalian social relationships, including parent-offspring recognition, mate recognition, and dominant-subordinate hierarchies. All of these behavioral processes require social discrimination which is a specific type of memory that differs from other types of learning and memory and may be subserved by distinct anatomical and neurochemical circuits in the brain. While humans and non-human primates rely primarily on visual and auditory cues for individual recognition, many other mammals rely on olfactory or pheromonal cues to differentiate individuals. The neural processing of these olfactory cues is critical to social memory and is dependent on the integrity of the neuropeptide systems for oxytocin (OT) and vasopressin (AVP). While many peptides may serve as important pheromonal cues in mammalian and non-mammalian species, OT and AVP are critical to the mammalian ability to processes such cues in an appropriate manner.
OT and AVP are closely related nonapeptides. They are transcribed from adjacent genes and differ by only two amino acids, suggesting that they arose from an ancestral gene by gene duplication. They are produced in discrete regions of the brain and are released both centrally into the brain, and peripherally into the circulation. OT and AVP destined for peripheral release is made in the magnocellular neurons of the paraventricular nucleus (PVN) and supra-optic nucleus (SON) of the hypothalamus and released into the bloodstream by the posterior pituitary. Peripherally, OT acts in the uterus to facilitate parturition and in the breast to facilitate milk ejection during lactation. AVP, also know as anti-diuretic hormone (ADH), acts in the kidney to facilitate re-absorption of water and the blood vessels to regulate vascular tone [28]. Centrally, these peptides are produced in the parvocelluar cells of the PVN as well as in extra-hypothalamic sites [11]. Receptors for these peptides are found in a variety of specific regions of the brain suggesting that they may play many different roles centrally.
The majority of evidence for OT and AVP as social memory peptides comes from the considerable investigations in the rat and mouse. The role of these neuropeptides in more complex forms of social memory, particularly in parent-offspring bonds in sheep and pair bonding in voles has also been well established. Through the use of pharmacological agents, transgenics, and viral vectors the specific roles and brain regions involved in peptide mediated social cognition is being elucidated. OT and AVP have been shown to be critical in the olfactory processing of social cues at many levels of the olfactory circuit and throughout the brain. Furthermore, OT and AVP mediated social memory can be quite potent lasting from 1 hour in rodents to a lifetime in voles. This review will cover the evidence for OT and AVP in rodent social recognition as well as offspring recognition in sheep and mate preference in pair bonding voles.
Section snippets
Social recognition in rodents
Social recognition tests are a group of learning and memory tasks that were originally created as a non-aversive alternative to the avoidance paradigms that had been traditionally used to examine learning and memory behaviors [57]. While social recognition is a model of learning and memory, these tests have more recently illustrated the unique aspects of social cognition. Social recognition tests make use of the animals’ natural tendency towards olfactory investigation of novel conspecifics.
Social recognition in complex social behaviors
Historically, social recognition has been studied in rats and mice and has been defined as the ability to recognize a familiar conspecific over a relatively short period of time. While OT and AVP can increase the duration of social recognition, this type of social memory is still considered short-term. There are other examples of social recognition in other species that are more enduring and can be considered permanent social memories. OT and AVP are critical in these diverse and more complex
Conclusions
Social recognition is critical for the formation and maintenance of all social relationships. The social behaviors of mammalian species varies greatly; however, social cognition forms the basis for both simple and complex social behaviors and OT and AVP play a fundamental role in the ability to form and retain these memories. Rats and mice use social recognition to recognize a familiar conspecific. Ewes use social memory to form the critical memory of their offspring; prairie voles use social
Acknowledgements
Manuscript supported by NIH MH070112 to IFB, MH56897, MH056538, and MH64692 to LJY, and NSF STC IBN-9876754 and the Yerkes Center Grant RR00165.
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