Abstract
Early experiences can alter adaptive emotional responses necessary for social behavior as well as physiological reactivity in the face of challenge. In the highly social prairie vole (Microtus ochrogaster), manipulations in early life or hormonal treatments specifically targeted at the neuropeptides oxytocin (OT) and arginine vasopressin (AVP), have long-lasting, often sexually dimorphic, consequences for social behavior. Here we examine the hypothesis that behavioral changes associated with differential early experience, in this case handling the family during the first week of life, may be mediated by changes in OT or AVP or their brain receptors. Four early treatment groups were used, differing only in the amount of manipulation received during the first week of life. MAN1 animals were handled once on post-natal day 1; MAN1 treatment produces a pattern of behavior usually considered typical of this species, against which other groups were compared. MAN1–7 animals were handled once a day for post-natal days 1–7, MAN 7 animals were handled once on post-natal day 7, and MAN0 animals received no handling during the first week of life. When tested following weaning, males in groups that had received manipulation during the first few days of life (MAN1 and MAN1–7) displayed higher alloparenting than other groups. Neuroendocrine measures, including OT receptor binding and OT and AVP immunoreactivity, varied by early treatment. In brain areas including the nucleus accumbens, bed nucleus of stria terminalis and lateral septum, MAN0 females showed increased OT receptor binding. MAN1 animals also displayed higher numbers of immunoreactive OT cell bodies in the supraoptic nucleus. Taken together these findings support the broader hypothesis that experiences in the first few days of life, mediated in part by sexually dimorphic changes in neuropeptides, especially in the receptor for OT, may have adaptive consequences for sociality and emotion regulation.
Highlights
The role of early experience in the development of adult behavior and psychopathology has been of considerable interest to neurobiologists for decades (Harlow, 1961, 1964; Harlow and Suomi, 1971; Hofer, 1978, 2006; Plotsky, 1997, 2002; Levine, 2002a)
Alloparental Behavior When groups that were manipulated before day 7 (MAN1 and MAN1–7) were combined and compared to groups that were not manipulated before day 7 (MAN0 and manipulation was postponed until postnatal day 7 (MAN7)), they differed significantly in alloparental behavior
Differential early handling experiences in prairie voles were associated with long-term, sexually dimorphic changes in social and anxiety-related behaviors, as well as neuroendocrine parameters
Summary
The role of early experience in the development of adult behavior and psychopathology has been of considerable interest to neurobiologists for decades (Harlow, 1961, 1964; Harlow and Suomi, 1971; Hofer, 1978, 2006; Plotsky, 1997, 2002; Levine, 2002a). Neglect or traumatic experiences may increase vulnerability in later life, contributing to the symptoms associated with depression, anxiety disorders, substance abuse, and post-traumatic stress disorder (Heim et al, 1997; Henry and Wang, 1998; Plotsky et al, 1998; Sanchez et al, 2001; Gilmer and McKinney, 2003; Advani et al, 2007; Francis and Kuhar, 2008). A rich literature chronicles the behavioral and physiological effects of early handling in rodents (Levine, 1957; Levine and Lewis, 1959b; Denenberg et al, 1962; Denenberg and Whimbey, 1963), focused on stress reactivity of the offspring (Levine, 2002b). Sex differences in the response to early handling are a consistent finding, these differences are not always in the same direction (Eklund and Arborelius, 2006; Slotten et al, 2006; Bales et al, 2007a; Renard et al, 2007; Aisa et al, 2008; Desbonnet et al, 2008)
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