The neurobiology of pair bonding: Insights from a socially monogamous rodent

Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA.
Frontiers in Neuroendocrinology (Impact Factor: 7.04). 01/2011; 32(1):53-69. DOI: 10.1016/j.yfrne.2010.07.006
Source: PubMed


The formation of enduring relationships between adult mates (i.e., pair bonds) is an integral aspect of human social behavior and has been implicated in both physical and psychological health. However, due to the inherent complexity of these bonds and the relative rarity with which they are formed in other mammalian species, we know surprisingly little about their underlying neurobiology. Over the past few decades, the prairie vole (Microtus ochrogaster) has emerged as an animal model of pair bonding. Research in this socially monogamous rodent has provided valuable insight into the neurobiological mechanisms that regulate pair bonding behaviors. Here, we review these studies and discuss the neural regulation of three behaviors inherent to pair bonding: the formation of partner preferences, the subsequent development of selective aggression toward unfamiliar conspecifics, and the bi-parental care of young. We focus on the role of vasopressin, oxytocin, and dopamine in the regulation of these behaviors, but also discuss the involvement of other neuropeptides, neurotransmitters, and hormones. These studies may not only contribute to the understanding of pair bonding in our own species, but may also offer insight into the underlying causes of social deficits noted in several mental health disorders.

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Available from: Kimberly Young, Aug 18, 2014
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    • "Indeed, social processes in young rodents are richly expressed at high levels and lend themselves toward ready delineation of neural substrates underlying social play behavior. Other rodent models, such as prairie voles, have been utilized extensively to better understand brain mechanisms underlying social bonding in young adults (Wang et al., 1998; Young et al., 2011). Social interaction in young adults is also commonly used as a reporter of sickness-like behavior as well as adverse consequences of stressor exposure (Arakawa et al., 2009; Christianson et al., 2009). "
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    ABSTRACT: Aging results in a natural decline in social behavior, yet little is known about the processes underlying these changes. Engaging in positive social interaction is associated with many health benefits, including reduced stress reactivity, and may serve as a potential buffer against adverse consequences of aging. The goal of these studies was to establish a tractable model for the assessment of social behavior deficits associated with late aging. Thus, in Exp. 1, 1.5-, 3-, and 18-month-old male Fischer 344 (F344) rats were assessed for object investigation, and social interaction with a same-aged partner (novel/familiar), or a different-aged partner, thereby establishing working parameters for studies that followed. Results revealed that 18-month-old males exhibited reductions in social investigation and social contact behavior, with this age-related decline not influenced by familiarity or age of the social partner. Subsequently, Exp. 2 extended assessment of social behavior to both male and female F344 rats at multiple ages (3, 9, 18, and 24 months), after which a series of sensorimotor performance tests were conducted. In this study, both males and females exhibited late aging-related reductions in social interactions, but these changes were more pronounced in females. Additionally, sensorimotor performance was shown to be impaired in 24-month-olds, but not 18-month-olds, with this deficit more evident in males. Finally, Exp. 3 examined whether aging-related inflammation could account for declines in social behavior during late aging by administering naproxen (0, 7, 14, and 28 mg/kg; s.c.)—a non-steroidal anti-inflammatory drug—to 18-month-old females. Results from this study revealed that social behavior was unaffected by acute or repeated (6 days) naproxen, suggesting that aging-related social deficits in females may not be a consequence of a general aging-related inflammation and/or malaise. Together, these findings demonstrate that aging-related declines in social behavior are (i) specific to social stimuli and (ii) not indicative of a general state of aging-related debilitation. Thus, these findings establish working parameters for a highly tractable model in which the neural and hormonal mechanisms underlying aging-related declines in social behavior can be examined.
    Full-text · Article · Jan 2016 · Experimental gerontology
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    • "Moreover, it has been suggested that oxy might exerts a role in the cognitive dysfunctions observed in alcoholics (Holden et al., 1988;Marchesi et al., 1997). All drugs of abuse increase dopamine release within the mesolimbic system (Pierce and Kumaresan, 2006) and Young and collaborators (Young et al., 2008Young et al., , 2011) demonstrated the existence of an interaction between oxy and dopaminergic system in both social and drug reward in prairie voles. In particular, the authors showed that methamphetamine was able to reduce pair bonding and pair bonding was able to reduce the rewarding properties of methamphetamine in prairie voles. "
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    ABSTRACT: Oxytocin (oxy) is a pituitary neuropeptide hormone synthesized from the paraventricular and supraoptic nuclei within the hypothalamus. Like other neuropeptides, oxy can modulate a wide range of neurotransmitter and neuromodulator activities. Additionally, through the neurohypophysis, oxy is secreted into the systemic circulation to act as a hormone, thereby influencing several body functions. Oxy plays a pivotal role in parturition, milk let-down and maternal behavior and has been demonstrated to be important in the formation of pair bonding between mother and infants as well as in mating pairs. Furthermore, oxy has been proven to play a key role in the regulation of several behaviors associated with neuropsychiatric disorders, including social interactions, social memory response to social stimuli, decision-making in the context of social interactions, feeding behavior, emotional reactivity, etc. An increasing body of evidence suggests that deregulations of the oxytocinergic system might be involved in the pathophysiology of certain neuropsychiatric disorders such as autism, eating disorders, schizophrenia, mood, and anxiety disorders. The potential use of oxy in these mental health disorders is attracting growing interest since numerous beneficial properties are ascribed to this neuropeptide. The present manuscript will review the existing findings on the role played by oxy in a variety of distinct physiological and behavioral functions (Figure 1) and on its role and impact in different psychiatric disorders. The aim of this review is to highlight the need of further investigations on this target that might contribute to the development of novel more efficacious therapies. Figure 1Oxytocin regulatory control of different and complex processes.
    Full-text · Article · Jan 2016 · Frontiers in Neuroscience
    • "Sociability is commonly tested using a three-chambered setup where rodents are presented and can chose to interact with a social stimulus (an unknown conspecific, a partner, etc.), with no stimulus (an empty chamber), or with a socially neutral stimulus (an inanimate object) (Crawley, 2000;Kaidanovich-Beilin, Lipina, Vukobradovic, Roder, & Woodgett, 2011;Moy et al., 2007;Roullet & Crawley, 2011;Young, Gobrogge, Liu, & Wang, 2011). It is argued that these tasks are relevant to social " drive " (i.e., motivation to engage in social interactions in p0135Bell, Bryson, & Lysaker, 1997), Facial Emotion Identification Test (Kerr & Neale, 1993), Pictures of Facial Affect (Ekman & Friesen, 1976), Facial Emotion Discrimination Test (Kerr & Neale, 1993), Videotape Affect Perception Test (Bellack, Blanchard, & Mueser, 1996), Vocal Emotion Identification Test (Kerr & Neale, 1993), Vocal Affect Recognition (Nowicki & Duke, 1994), Prosody task (Pijnenborg, Withaar, Bosch, & Brouwer, 2007). "
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    ABSTRACT: Cognitive impairments, especially in higher order cognitive functions, are core features of schizophrenia. Importantly, despite their early onset, long-lasting presence, and serious impact on the life quality of patients and their families, cognitive deficits are still mostly incurable and their specific causes are still unknown. In this context, mouse/rat models with cautious and well-designed translational valence constitute an invaluable instrument in dissecting the selective nature of schizophrenia-relevant cognitive deficits, including their genetic, environmental, and neuronal/cellular mechanisms. Moreover, these models are also crucial for the implementation of more effective therapeutical strategies. Thus, based on clinical evidence in schizophrenia, here we will specifically address cognitive domains such as executive control, working memory, attention, and social cognition. We first briefly present human tasks commonly used to measure each of these domains; thereafter, we describe relevant equivalent tasks developed and now available for use in rodents.
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