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Young_NN04 - REVIEW THE SEXUAL BRAIN 2004 Nature Publishing...

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Sexual attraction and the selective social attachments that often follow are two of the most powerful driving forces of human behav- ior, profoundly influencing art, music, literature and politics throughout history. The presence of strong, enduring relationships between sexual partners is widespread in nearly all societies, particu- larly in societies where monogamy is a predominant feature of the social organization. Whether humans have a biological propensity to practice monogamy (or perhaps more correctly, serial monogamy) is debatable; however, there is little doubt that the ability to form intense social attachments—or pair bonds—with a mate has a biolog- ical architecture with definable molecular and neural mechanisms. Studies using monogamous rodents as models for social attachment are providing insights into the biology of pair-bond formation. The term ‘monogamy’ implies a social organization in which a male and female mate exclusively with each other, although extra- pair copulations are not unusual in monogamous species 1 . For this reason, the term ‘monogamy’ is used here to refer to a social organi- zation in which each member of a mating pair displays selective (but not exclusive) affiliation and copulation, as well as nest sharing, with the partner; it also typically implies biparental care of offspring. Only 3–5% of mammals exhibit a monogamous social structure as defined by these criteria 2 . One group of species in particular, voles in the genus Microtus , has emerged as a valuable tool for investigating the neurobiological mechanisms of pair-bond formation 3,4 . Here we review recent discoveries concerning the molecular, cellular and neu- robiological pathways that result in the development of a pair bond in the monogamous prairie vole ( Microtus ochrogaster ). These stud- ies provide a framework for understanding the regulation and evolu- tion of complex social behavior and may provide insights into the human social brain. Peptidergic regulation of the pair bond Like humans, voles display a remarkable diversity in social organiza- tion. For example, prairie voles form enduring pair bonds and are biparental, but montane ( Microtus montanus ) and meadow ( Microtus pennsylvanicus ) voles are nonmonogamous and typically do not dis- play biparental care 5–7 . In nature, the majority of prairie voles that lose a mate never take on another partner 8 . In the laboratory, researchers study pair-bond formation using a partner-preference test. The testing apparatus consists of three cham- bers connected by tubes. The ‘partner’ and a novel ‘stranger’ are teth- ered in their own chambers, whereas the subject is free to move throughout the apparatus during a 3-h test. Pair bonding is inferred when subjects spend significantly more time in close proximity to the partner compared to the stranger (partner preference). In prairie voles, mating facilitates formation of partner preference, although cohabitation without mating may also result in partner-preference formation under some circumstances 9 .
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