Elsevier

Hormones and Behavior

Volume 58, Issue 3, August 2010, Pages 478-484
Hormones and Behavior

Agonistic encounters and brain activation in dominant and subordinate male greater long-tailed hamsters

https://doi.org/10.1016/j.yhbeh.2010.05.001Get rights and content

Abstract

During an agonistic encounter test, dominant male greater long-tailed hamsters (Tscheskia triton) initiated attacks sooner and displayed higher levels of aggression and flank marking behavior than their subordinate counterparts. Accordingly, subordinate males exhibited more defensive behavior than dominant ones. Specific patterns of neuronal activation, measured by Fos-immunoreactive staining (Fos-ir), were found in the hamster brain following agonistic interactions. Increased Fos-ir was observed in the bed nucleus of the stria terminalis (BST), ventromedial hypothalamus (VMH), and medial (MeA) and anterior cortical (ACo) nuclei of the amygdala (AMYG) in both dominant and subordinate males. In contrast, dominant males had significantly higher Fos-ir densities in the medial preoptic area (MPOA) than subordinate males, whereas subordinate males expressed higher densities of Fos-ir in the anterior hypothalamus (AH) and central nucleus of the amygdala (CeA). Additionally, Fos-ir levels in the MPOA were significantly correlated with aggression and Fos-ir levels in the AH and CeA were correlated with defensive behavior. Together, our data indicate distinct patterns of neuronal activation associated with agonistic encounters in a behavior-specific manner in male greater long-tailed hamsters.

Introduction

Agonistic behavior has been defined as adaptive aggressive and defensive actions that occur during a conflict between members of the same species (Scott and Fredericson, 1951). Agonistic encounters usually lead to the establishment of a dominant–subordinate hierarchy, which, in turn, plays an important role in socialization, resource acquisition, reproductive success, and even survival. Agonistic behavior has been examined in a variety of rodent species, including rats, mice, hamsters and voles, under different social contexts (Davis and Marler, 2004, Delville et al., 2000, Gammie and Nelson, 2001, Gobrogge et al., 2007, Haller et al., 2006, Veening et al., 2005). Although these studies have provided important information about agonistic behavior and its underlying neural mechanisms, the majority have focused exclusively on aggressive behavior (Delville et al., 2000, Gobrogge et al., 2007, Haller et al., 2006, Veening et al., 2005), while little attention has been paid to defensive behavior. Given that an agonistic encounter is a dynamic behavioral interaction involving both aggressive and defensive behaviors, each of which depend upon the other, it is essential to examine the entire repertoire of behaviors displayed during agonistic interactions. Such information could offer insight into whether aggressive and defensive behaviors represent opposite ends of a single behavioral continuum regulated by a complex neural circuit, or alternatively, represent two independent behavioral patterns that could be regulated by distinct, but well integrated, neural circuits (Adams, 1979, Adams, 2006, Ramirez et al., 1988).

The greater long-tailed hamster (Tscheskia triton) is a solitary, polygamous rodent species that lives in the farmlands of Northern China (Yang et al., 1996, Zhang et al., 2001a, Zhang et al., 2001b). Previous studies have shown that males of this species display intense agonistic interactions during same-sex encounters, and such interactions typically result in a clearly identifiable dominant versus subordinate status, with the dominant animal displaying more aggression and the subordinate animal displaying a higher level of defensive behavior (Wang et al., 2009, Zhang et al., 2001b). Although circulating levels of hormones (e.g., testosterone and corticosterone) have been implicated in such agonistic encounters (Wang et al., 2009, Zhang et al., 2001a, Zhang et al., 2001b), the underlying neural substrates are still unknown. In the present study, we tested the hypothesis that agonistic behavior correlates with patterns of neuronal activation in the brain in a behavior-specific manner. We compared behavioral patterns of dominant versus subordinate male hamsters during agonistic encounters, used the protein product (Fos) of an immediate early gene, c-fos, to map related neuronal activation in the brain, and correlated agonistic behaviors with regional neuronal activation in male greater long-tailed hamsters.

Section snippets

Subjects

Subjects were sexually naïve adult male greater long-tailed hamsters (Tscheskia triton) that were F1 offspring of a laboratory breeding colony originating from field captured animals. The hamsters were weaned at 25 days of age and housed individually in plastic cages (27 × 16 × 13 cm) that contained wood shavings as bedding. Food and water were provided ad libitum. All cages were maintained under a reversed light/dark cycle (16 L:8D with lights on at 1700). Temperature was maintained at 20 ± 2 °C. All

Behaviors

The dominant–subordinate status was determined rapidly (fleeing latency: 68.4 ± 29.1 s) after pairing the two males, and once established, the relationship remained consistent throughout the entire 10-min behavioral test. Dominant males displayed higher levels of aggression, compared to their subordinate counterparts, as indicated by a shorter latency to initiate attacks (Z = 1.99, p < 0.05; Fig. 1B) and a higher frequency (Z = 2.21, p < 0.05) and duration (Z = 2.20, p < 0.05) of aggression, whereas

Discussion

In the present study, we found that agonistic encounters between male greater long-tailed hamsters resulted in the establishment of a dominant–subordinate relationship with dominant males displaying flank marking, initiating attack sooner, and showing more aggression and subordinates displaying more defensive behavior and fleeing. Such behavioral interactions resulted in significant neuronal activation, as indicated by Fos-ir in selected brain areas. Most interestingly, discrete patterns of

Acknowledgments

This research was supported by grants from the National Basic Research Program of China (2007BC109101) and The Chinese Academy of Sciences (KSCX2-YW-N-06) to ZBZ and NIMH R01-58616 to ZXW.

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