Social buffering in rats: prolactin attenuation of active interaction.

Previous research has identified that social partners buffer stress (Kikusui, Winslow, & Mori, 2006). Several mechanisms of this social buffering effect are being identified (Kiyokawa, Kikusui, Takeuchi, & Mori, 2004; Wilson, 2007 3). The purpose of the current study was to use a rat model to examine the role of touch by a social partner to decrease stress responses when exposed to a conditioned emotional response (CER) stressor. In humans, stress occurs when an internal need or environmental demand is viewed as threatening or out of one’s control (Clark, Rager, & Calpin, 1997). Stressors are often categorized as either physical or psychological. Physical stress is defined as a threat based on physical harm, pain, or the capacity to terminate life (Lovallo, 1997). This type of stress is experimentally induced in animal research by methods which include, but are not limited to, restraint (Kant, Eggleston, Landman-Roberts, Kenion, Driver, & Meyerhoff, 1985; Kant, Mougey, & Meyerhoff, 1986; Orr, Meyerhoff, Mougey, & Bunnell, 1990; Wilson, McKinley, & Young, 2000; Klenerova, Sida, Hynie, & Jurcovicova, 2001), forced swim (Greisen, Altar, Bolwig, Whitehead, & Wortwein, 2005; Ma, Shipston, Morilak, & Russell, 2005), and footshock (Huhman, Mougey, Moore, & Meyerhoff, 1995; Pitman, Natelson, Ottenweller, McCarty, Pritzel, & Tapp, 1995; Maslova, Bulygina, & Markel, 2003; Westenbroek, Ter Horst, Roos, Kuipers, Trentani, & den Boer, 2003; Penka, Bond, & Heinrichs, 2004). Psychological stressors are defined as situations perceived as threatening, and this interpretation leads to the engagement of a stress response regardless of whether the environment is actually harmful (Clark, et al, 1997). Psychological stress is commonly induced in animal research by methods such as open-field exposure or a novel environment (Yelvington, Weiss, & Ratner, 1985; Muir & Pfister, 1986; Terranova, Cirulli, & Laviola, 1999; Wilson, 2000, 2001; Miserendino, Haile, & Kosten, 2003; Pijlman, Wolterink, & Van Ree, 2003), elevated plus maze (Belda, Marquez, & Armario, 2004; Mueller, Dolgas, & Herman, 2004; Marquez, Nadal, & Armario, 2005), and conditioned fear (Van de Kar, Lorens, McWilliams, Kunimoto, Urban, & Bethea, 1984; Przewlocka, Sumova, & Lason, 1990; Zhu & Onaka, 2003). Conditioned fear offers an animal model of stress based on prior experience. Female animals rarely have been examined in the CER stress literature; the conditioned-fear paradigm previously relied almost exclusively on male rats (Van de Kar, Lorens, Urbana, Richardson, Paris, & Bethea, 1985; Paris, Lorens, Van de Kar, Urban, Richardson-Morton, & Bethea, 1987; Lorens, Hata, Handa, Van de Kar, Guschwan, Goral, et al., 1990). Therefore, one goal of the present study was to include female rats in the sample testing the animal model of learned stress based on prolactin responses to stress. Previous research found prolactin secretion to increase in response to both physical and psychological stressors (Telner, Merali, & Singhal, 1982; Yelvington, et al., 1985; Paris, et al., 1987; Marti-Carbonell, Darbra, Garau, Sanz, & Balada, 1993). Prolactin increases as a direct function of stimulus intensities (Armario, Lopez-Calderon, Jolin, & Castellanos, 1986). Orr, et al. (1990) found tailshock to be more intense than immobilization, and immobilization more intense than exposure to a chamber without shock. Different intensities of the same stressor indicate gradations in the prolactin response. For example, Kant and colleagues found prolactin sensitive to increasing footshock intensities (Kant, Mougey, Pennington, & Meyerhoff, 1983). Based on these studies, rats were expected to display differences in prolactin across slight environmental variations even when exposed to the same stressor. Responses to psychological stressors may be alleviated by social support, allowing the presence of another to act as a buffer against perceived threats (Bondi & Picardi, 1999). Among squirrel monkeys in a large social group, exposure to a caged live boa constrictor did not increase adrenocortical activities; however, the same stressor experienced in the absence of social partners induced elevated hormonal levels in squirrel monkeys (Coe, Franklin, Smith, & Levine, 1982). A similar effect was found in prolactin levels of rats exposed to an open-field stressor, with and without a social partner. Juvenile male and female rats exposed to a novel environment in the presence of a conspecific had significantly lower levels of prolactin than control rats individually exposed to the same stressor (Wilson, 2000). In this study, stress responses appeared to attenuate given the presence of a conspecific. However, the presence of a conspecific may have offered a distraction from the stressful environment. The present study included a condition with a novel object in the chamber to examine this possibility. In addition to possible distraction, the conspecific offered active touch, which may be an important element in social buffering (Wilson, 2001). In a previous study, juvenile rats which were allowed to touch during an open-field stressor had lower levels of prolactin than rats not allowed to touch, even though all animals were able to see, hear, and smell the conspecific (Wilson, 2001). Although touch may indeed promote social buffering, one does not know if active touch is necessary. That is, the occurrence of social buffering may rely on reciprocated touch with an active animal, or it may rely simply on tactile stimulation. The exploration of comfort and tactile stimulation provided by living and nonliving stimuli dates back to Harlow’s research (e.g., 1959). In the present study, the experimental animals were exposed to live and euthanized conspecifics to explore the function of touch in social buffering. Live conspecifics reciprocated touch, and euthanized conspecifics functioned as tactile stimulation which received touch without response. Increased touch may be confounded by increased activity, and activity has been associated with lower levels of prolactin (Marti-Carbonell, et al., 1993; Wilson, 2000). Similarly, application of prolactin to the ventral hippocampus in female rats decreased ambulation (Alvarez & Banzan, 1994). In the present study, active touch associated with a live conspecific could be particularly problematic, as it would offer an alternative explanation for hypothesized reductions in prolactin. Therefore, to analyze general activity, freezing behaviors were quantified. When subjects are exposed to the conditioned emotional response (CER) paradigm, subsequent exposures evoke a freeze behavior in anticipation for the shock. Freezing does not allow the rat to engage in alternative active behaviors. In the present study, rats were conditioned to fear a chamber by pairing the environment with footshock to produce a conditioned emotional response on the day of testing. Experimental conditions consisted of animals tested alone (Alone), animals paired with a novel object (Object), animals paired with a recently euthanized conspecific (Euthanized), and animals paired with a live social conspecific (Social). A fifth condition consisted of rats which were never conditioned to fear the chamber due to shock but were conditioned to the novel atmosphere of the chamber. These rats were tested alone on the day of experimentation and served as the control condition. The Alone, Object, and Euthanized experimental conditions were expected to show higher levels of prolactin than the Control condition. The Social condition (rats tested with an interactive littermate) was expected to exhibit prolactin levels similar to those of the Control condition and lower levels of prolactin than the Alone condition (animals exposed to the CER paradigm alone). Although activity was not expected to differ across treatment conditions, it was expected that touch would be enhanced in the Social condition.