Karelina et al H&B 2010

Estrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species Kate Karelina a, ⁎, James C. Walton a , Zachary M. Weil a,1 , Greg J. Norman b , Randy J. Nelson a,b,c , A. Courtney DeVries a,b,c a Department of Neuroscience, Ohio State University, Columbus, OH 43210, USA b Department of Psychology, Ohio State University, Columbus, OH 43210, USA c Institute for Behavioral Medicine Research, Ohio State University, Columbus, OH 43210, USA a b s t r a c t a r t i c l e i n f o Article history: Received 14 January 2010 Revised 20 March 2010 Accepted 31 March 2010 Available online 9 April 2010 Keywords: Peromyscus californicus Peromyscus leucopus Social behavior Oxytocin Corticosterone The social organization of rodent species determines behavioral patterns for both af liative and agonistic encounters. The neuropeptide oxytocin has been implicated in the mediation of social behavior; however, varia bilit y in both neurope ptid e expr essio n and soci al beha vior within a sing le spec ies indicate s an additional medi ating factor. The purp ose of the prese nt comp arati ve stud y was to inves tigat e socia l beha viors in naïve mixed-s ex pairs of mono gamo us Peromyscus californicus and polygynous Peromyscus leucopus. We identied substantial inter- and intra-specic variability in the expression of af liative and agonistic behaviors. Although all P. californicus tested engaged in frequent and prolonged intervals of social contact and rarel y enga ged in aggr essiv e beha vior s, P. leuco pus exhibited signicant variability in both measures of social behaviors. The naturally occurring differences in social behavior displayed by P. leucopus vary across the estrous cycle, and correspond to hypothalamic oxytocin, as well as circulating oxytocin and glucocorticoid concentrations. These results provide evidence for a rhythm in social behavior across the estrous cycle in polygynous, but not monogamous, Peromyscus species. © 2010 Elsevier Inc. All rights reserved. Introduction Mammals display a variety of social systems, ranging from the monoga mous to highly promisc uous. Alth ough the majo rity of mammalian species exhibit a polygynous social system, a substantial mino rity of soci ally mono gamou s mammals have been iden tied (Donaldson and Young, 2008). Extensive insight into the neurobio- logical correlates of social behavior has been made possible through comparison of closely related rodent species that exhibit different social systems (Carter et al., 1995; DeVries et al., 1995; Young, 2002; Young et al., 2001). For example, soci ally mono gamou s Calif orni a mice (Peromyscus californicus) form long-lasting pair-bonds, engage in bipa rental beha viors , and exhi bit aggre ssiv e behav ior towar d unknown same-sex conspeci cs (Gubernick and Alberts, 1987). In contrast, closely related but socially polygynous white-footed mice (Peromyscus leucopus) typ ica llydo not for m pai r bon ds,exhib it mos tly uniparental behavior, and are less likely to engage in territorial or conspeci c aggression (Bester-Meredith et al., 1999). Studies of closely related rodent species have demonstrated a role for the neuropeptide oxytocin (OT) as an important inuence in the development and maintenance of social behaviors. There are distinct diff eren ces in OT receptor (OTR ) dist ributio n between soc iall y monog amou s and polyg ynous species ( Insel and Shapi ro, 1992 ). Indeed, OTR density is elevated in the nucleus accumbens, lateral septum, and hypothalamus of monogamous vol e specie s and correlates with af liative behaviors in general and parental behaviors in particular (Francis et al., 2002; Insel and Shapiro, 1992; Ross et al., 2009). Early studies indicated that intracerebroventricular adminis- tra tion of OT fac ili tat es the onset of af liat ive soci al beha viors , incl uding female sexu al rece ptivi ty (Gre er et al. , 1986), paren tal behavior (Pedersen and Prange, 1979), and pair-bonding (Cho et al., 1999; Wi lli ams et al. , 1992). In con tra st, treat men t wit h an OT receptor antagonist or antisense oligodeoxynucleotides decreases or eliminat es thes e beha viors (McCa rthy et a l., 1994 ; Young et a l., 2001 ), indicatin g a ce ntr al role of OT in af liative behavior. Converging evidence from OT knockout studies in mice provides further support for a role of OT in maintaining social behaviors; OT knockout mice fail to dev elo p socialmemor y, but this decit is resc ued by admi nist ration of OT (Ferguson et al., 2000). Several of the behavioral effects of OT are modulated by ovarian steroids (Cushin g andKramer, 200 5; McC art hy et al. , 199 4; Yamamo to et al., 2006). The expression of maternal behavior, including maternal aggression, following OT administration in rodents is facilitated by Hormones and Behavior 58 (2010) 193–199 ⁎ Corresponding author. Department of Neuroscience, Ohio State University, 750 Biomedical Research Tower, 460 W 12th Ave., Columbus, OH 43210, USA. Fax: +1 614 292 3464. E-mail address: [email protected] (K. Karelina). 1 Current Addre ss: Labor ator y of Neur obio logy and Beha vior and Labo rato ry of Neuroendocrinology , Rockefeller University, New York, NY 10065, USA. 0018-506X/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2010.03.022 Contents lists available at ScienceDirect Hormones and Behavior j ou r n a l home p a g e: www.else v i e r. c o m/l o cat e / y h b e h

Karelina et al H&B 2010

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