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Am J Physiol Regul Integr Comp Physiol 292: R283-R290, 2007. First published August 31, 2006; doi:10.1152/ajpregu.00330.2006
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APPETITE, OBESITY, DIGESTION, AND METABOLISM

Social defeat and footshock increase body mass and adiposity in male Syrian hamsters

Matia B. Solomon,1,3 Michelle T. Foster,2,3 Timothy J. Bartness,1,2,3 and Kim L. Huhman2,3

1Department of Psychology, 2Department of Biology, and 3Center for Behavioral Neuroscience, Georgia State University, Atlanta, Georgia

Submitted 16 May 2006 ; accepted in final form 23 August 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Obesity is a world-wide epidemic, and many factors, including stress, have been linked to this growing trend. After social stress (i.e., defeat), subordinate laboratory rats and most laboratory mice become hypophagic and, subsequently, lose body mass; the opposite is true of subordinate Syrian hamsters. After social defeat, Syrian hamsters become hyperphagic and gain body mass compared with nonstressed controls. It is unknown whether this increase in body mass and food intake is limited to subordinate hamsters. In experiment 1, we asked, do dominant hamsters increase food intake, body mass, and adiposity after an agonistic encounter? Subordinate hamsters increased food intake and body mass compared with nonstressed controls. Although there was no difference in food intake or absolute body mass between dominant and nonstressed control animals, cumulative body mass gain was significantly higher in dominant than in nonstressed control animals. Total carcass lipid and white adipose tissue (WAT) (i.e., retroperitoneal and epididymal WAT) masses were significantly increased in subordinate, but not dominant, hamsters compared with nonstressed controls. In experiment 2, we asked, does footshock stress increase food intake, body mass, and adiposity. Hamsters exposed to defeat, but not footshock stress, increased food intake relative to nonstressed controls. In animals exposed to defeat or footshock stress, body mass, as well as mesenteric WAT mass, increased compared with nonstressed controls. Collectively, these data demonstrate that social and nonsocial stressors increase body and lipid mass in male hamsters, suggesting that this species may prove useful for studying the physiology of stress-induced obesity in some humans.

stress; subordinate; aggression; agonistic; leptin; insulin; obesity

OBESITY IS A WORLD-WIDE EPIDEMIC with comorbidities such as cardiovascular disease, type 2 diabetes, hypertension, depression, and certain forms of cancer (8, 20, 43). Because obesity is associated with these and other pathologies, investigation of the underlying psychosocial and physiological factors that may account for this growing trend is critical. The underlying mechanisms for the increases in obesity involve increases in energy intake and/or decreases in energy expenditure, which have, as their bases, genetic and/or environmental influences. Stress is one environmental influence that has been associated with obesity (9), although it receives considerably less scientific attention than the more frequently studied environmental factor, high-calorie diets.

A variety of animal models incorporating both nonsocial and social stressors have been used to reveal the relations among stress, food intake, and adiposity. Mild, nonsocial stressors, such as tail pinch, brief restraint, and handling, increase food intake in laboratory rats (2, 33). By contrast, chronic footshock, chronic restraint, and chronic noise stress decrease food intake and body mass (1, 22, 30, 42, 46). The extent of the decrease in food intake and body mass depends on several factors, including the intensity of the stressor (36), time of day (23, 44, 46), and diet composition (24). Nonsocial stressors, such as restraint and footshock, often are preferred in experimental studies over more complex social stressors, such as agonistic behavior (i.e., behavior that is exhibited during social conflict between conspecifics), because greater control of the intensity, duration, and frequency of the nonsocial stressor yields less variable responses to stress and, hence, more easily replicable results.

One naturally occurring form of social stress typically observed after an agonistic interaction in rodents, humans, and nonhuman primates is social defeat (7, 45, 47, 48). In the laboratory, social defeat typically is induced using the resident-intruder model, whereby an intruder conspecific is placed into the home cage of a larger resident and the intruder usually is defeated by the resident aggressor. The effects of social defeat on food intake and body mass have been studied extensively in laboratory rats and mice. In most studies, subordinate rats and mice decrease their food intake and either decrease their body mass or have an attenuated body mass gain compared with their nonstressed control and/or dominant counterparts (3, 10, 14, 21, 28, 29, 37, 47). In some isolated cases, however, body mass is increased in subordinate laboratory rats and mice compared with their nonstressed control or dominant counterparts (6, 50). The reason for these discrepant body mass and food intake responses after social defeat is unknown, but they could be due to differences in rat strains (i.e., Wistar vs. Long Evans rats) or the duration and intensity of the defeat episodes. Overall, however, the predominant response of laboratory rats and mice to social stress is inhibition of food intake and growth of body and lipid mass.

In contrast to most laboratory rats and mice, in Syrian hamsters (Mesocricetus auratus), social stress appears to trigger increases in food intake and body and lipid masses. This was first noted in group-housing conditions, where female Syrian hamsters increase their food intake and body and lipid mass compared with their singly housed counterparts (11, 18, 38). Because Syrian hamsters naturally are a solitary species and are highly territorial (40), it may be that group housing is a social stressor for these animals. In the earlier studies of group-housed hamsters, no attempt was made to distinguish between dominant and subordinate animals. It is possible that there is a difference in body and lipid mass and food intake depending on social status in these group-housing conditions.

Recently, we demonstrated significant increases in food intake and body and fat pad masses in subordinate male hamsters after agonistic encounters compared with nonstressed controls (17); however, we did not test whether the stress-induced increases in food intake, body mass, and adiposity also occurred in dominant hamsters. Therefore, the purpose of the present study was to determine 1) whether dominant and subordinate hamsters increase food intake, body mass, and adiposity after an agonistic encounter and 2) whether exposure to a nonsocial stressor, footshock, increases these measures as well. In experiment 1, we measured food intake and body and lipid masses in subordinate and dominant hamsters after an agonistic encounter as well as in their nonstressed controls. In experiment 2, we measured food intake and body and lipid masses in hamsters after exposure to social defeat or footshock stress as well as in their nonstressed controls. In experiment 1, we asked, do dominant male hamsters increase food intake, body mass, and adiposity after an agonistic encounter? In experiment 2, we asked, does footshock stress increase food intake, body mass, and adiposity in male Syrian hamsters?


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Animals and Housing Conditions

Male Syrian hamsters (Charles River Laboratories) were ~10 wk old and weighed 120–125 g at the beginning of the study. On arrival from the supplier, hamsters were individually housed in polycarbonate cages (20 x 40 x 20 cm) with wire mesh tops and Alpha Dri bedding (Shepherd Specialty Papers, Kalamazoo, MI) in a temperature-controlled vivarium with a 14:10-h light-dark cycle (lights off at 1100 Eastern Standard Time). Hamsters were given food (PMI Rodent Diet no 5001, St. Louis, MO) and water ad libitum, except during the agonistic encounters. All procedures and protocols were approved by the Georgia State University Institutional Animal Care and Use Committee and are in accordance with Public Health Service and US Department of Agriculture guidelines.

Food Intake and Body Mass

Beginning 1 wk before the start of each experiment, food intake and body mass were measured (corrected for spillage and pouching) daily at 1000 to within 0.01 g; this procedure continued daily throughout both experiments.

Experiment 1: Do Dominant Male Hamsters Increase Food Intake, Body Mass, and Adiposity After an Agonistic Encounter?

Agonistic encounters. Twenty-seven hamsters were matched for body mass and assigned to control (n = 9), resident (n = 9), and intruder (n = 9) groups. On the days when hamsters were exposed to the social stressor, all hamsters (including the nonstressed controls) were transported from the vivarium to the behavioral room for pairing. The controls remained in their home cages during the agonistic encounters. All encounters occurred during the first 2 h of dark onset. A resident-intruder model was used to reliably induce social conflict: one hamster (the intruder) was placed into the home cage of its opponent (the resident). The purpose of the experiment was to examine the effects of the agonistic encounter on body mass, food intake, and adiposity in subordinate (i.e., losers) and dominant (i.e., winners) animals; therefore, the animals were divided into winners and losers irrespective of territorial status. All encounters were 7 min in duration and took place over 4 consecutive days. The purpose of one additional encounter, 1 wk after the fourth agonistic encounter, was to assess whether the dominant-subordinate relationship was stable over time. All agonistic encounters were videotaped.

Blood collection and fat pad and testes harvesting. All animals had ad libitum access to food before decapitation; however, because Syrian hamsters eat approximately every 4 h (12), the impact of recently eaten food on hormones and metabolic measures is minimized compared with laboratory rats and mice.

At the end of the study, trunk blood was collected after rapid decapitation. Serum was obtained from blood that was collected and refrigerated overnight. Samples were spun in a refrigerated centrifuge at 2,000 g for 20 min at 8°C, and the serum was stored in polypropylene microcentrifuge tubes at –20°C.

Immediately after trunk blood collection, white adipose tissue (WAT) pads, including the mesenteric WAT (MWAT), epididymal (EWAT), retroperitoneal (RWAT), and inguinal (IWAT) subcutaneous fat pads, were harvested. Fat pads and testes were weighed and returned to the carcass for later analysis of carcass composition.

Radioimmunoassay of leptin and testosterone. Leptin and testosterone (T) serum assays were performed in duplicate by the Endocrine Core Laboratory, Yerkes Regional Primate Research Center of Emory University, using commercially prepared kits for murine leptin and rat T (Diagnostic Systems Laboratories, Webster, TX). Sensitivities of the assays were 0.08 and 0.05 ng/ml for T and leptin, respectively. Intra-assay variability was <10% for both assays, and all samples were run in the same assay.

Carcass composition. The carcasses were processed for carcass composition analysis according to the method of Leshner et al. (31). Briefly, the shaved, eviscerated carcasses were dried to a constant weight at 85°C for gravimetric determination of total carcass water. The dehydrated carcasses were finely ground, and lipid content was determined gravimetrically by extraction using petroleum ether. Fat-free dry mass (FFDM) was determined as follows: carcass wet weight – (total carcass water + total carcass lipid).

Experiment 2: Does Footshock Stress Increase Food Intake, Body Mass, and Adiposity in Male Syrian Hamsters?

Twenty male hamsters were matched for body mass and then assigned to the defeat (n = 7), footshock (n = 7), and control (n = 6) groups. Testing for the defeat and footshock groups took place within 2 h after dark onset as in experiment 1. On the day of testing, all animals were transported from the vivarium to the behavioral testing rooms. The control groups remained in their home cages during the stress procedure. Briefly, the defeat group was placed in the home cage of trained resident aggressors for 7 min over 4 consecutive days. The resident aggressors were larger animals that were known to be aggressive, and, in all cases, the resident aggressors rapidly became dominant over the experimental animals.

The footshock group was placed in a standard shock box: 91 x 15 x 20 cm (length x height x width) at the top and 6.4 cm wide at the bottom. Animals were subjected to six intermittent, 5-s scrambled 1-mA footshocks over 7 min via the electrified metallic floor of the box for a total footshock duration of 30 s. After each session, the footshock box was cleaned with a 70% (vol/vol) ethanol solution to minimize remaining odors. We used a 1-mA footshock, which was shown in previous research from our laboratory to be sufficient to elicit a hormonal stress response in male Syrian hamsters (26).

Blood collection and fat pad and testes harvesting. Trunk blood was collected and fat pads and testes were harvested as described in experiment 1.

Radioimmunoassay of leptin and insulin. Assays for serum leptin and insulin were performed in duplicate by the Endocrine Core Laboratory, Yerkes Regional Primate Research Center of Emory University, using a commercially prepared kit for murine leptin and rat insulin (Diagnostic Systems Laboratories). Sensitivities were 0.05 and 0.07 ng/ml for the leptin and insulin assays, respectively. Intra-assay variability was <10% for both assays, and all samples were run in the same assay.

Carcass composition. Carcass composition was determined as described in experiment 1.

Statistical Analyses

Data were analyzed using SPSS for Windows (release 11.5.0, SPSS, Chicago, IL). For experiments 1 and 2, the effect of experimental treatment on body mass and food intake was determined by repeated-measures AVOVA, with experimental treatment as the between-subjects factor and time (i.e., day) as the within-subjects factor. The effects of experimental treatment on hormones, fat pad masses, and carcass composition were analyzed by one-way ANOVA, with experimental treatment as the fixed factor, followed by least significant difference post hoc tests. Differences among the groups were considered statistically significant if P < 0.05. Exact probabilities and test values are omitted for simplicity and clarity in the presentation of the results.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
Experiment 1: Do Dominant Male Hamsters Increase Food Intake, Body Mass, and Adiposity After an Agonistic Encounter?

Body mass, food intake, and feed efficiency. At ~1 wk after the last agonistic encounter and throughout the experiment, body mass was significantly increased in subordinate hamsters compared with the nonstressed controls (P < 0.05; Fig. 1A). There was no significant difference in absolute body mass between subordinate and dominant animals across the experiment (Fig. 1A). Although there was no significant difference in absolute body mass between dominant and nonstressed control hamsters, cumulative body mass gain was significantly greater in dominant than in nonstressed control animals (P < 0.05; Fig. 1B; cumulative body mass gain = final body mass – baseline body mass).


Figure 1
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  		Fig. 1. A: absolute body mass of control (n = 9), subordinate (n = 8), and dominant (n = 9) male hamsters over 25 days in experiment 1. Arrows, days of agonistic encounters between subordinate and dominant groups only (i.e., days 6, 7, 8, 9, and 16). B: cumulative body mass increase relative to baseline in control (n = 9), subordinate (n = 8), and dominant (n = 9) male hamsters in experiment 1. Values are means ± SE. *Significant difference between subordinate and control only (P < 0.05). Nonshared letters (a, b, c) indicate statistically significant differences (P < 0.05).

 
One nonstressed control and one subordinate animal were eliminated from the food intake analysis because of excessive shredding of food, which made it difficult to gather accurate food intake measurements. At <1 wk after the last agonistic encounter (day 16), subordinate male hamsters began eating significantly more food than nonstressed controls (P < 0.05; Fig. 2). There was no significant difference in cumulative food intake between dominant and nonstressed control animals; similarly, there was no difference in food intake between subordinate and dominant groups (Fig. 2). Feed efficiencies (cumulative body mass gain ÷ cumulative amount of food consumed during entire experiment) were significantly higher in subordinate male hamsters than in nonstressed control and dominant hamsters (P < 0.05 for each; Fig. 3). Feed efficiency was significantly higher in dominant than in nonstressed control hamsters (P < 0.05; Fig. 3).


Figure 2
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  		Fig. 2. Cumulative food intake of control (n = 8), subordinate (n = 7), and dominant (n = 9) hamsters in experiment 1. Arrows, days of agonistic encounters between subordinate and dominant groups only (i.e., days 6, 7, 8, 9, and 16). Values are means ± SE. *Significant difference between subordinate and control only (P < 0.05).

 

Figure 3
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  		Fig. 3. Feed efficiency of control (n = 8), subordinate (n = 7), and dominant (n = 9) hamsters. Values are means ± SE. Nonshared letters (a, b, c) indicate statistically significant differences (P < 0.05).

 
Agonistic behavior. Throughout the study, once a dominant-subordinate relationship was established, it remained stable throughout the study. In approximately half (4 of 9) of the pairs, the intruders became dominant over the residents. These data indicate that, in studies where hamsters are matched by body mass, resident status is not a reliable predictor of dominance (data not shown).

Fat pad and testes mass. MWAT, IWAT, RWAT, and EWAT masses were significantly increased in subordinate hamsters compared with the dominant hamsters (P < 0.05 for each; Fig. 4). RWAT and EWAT masses were significantly increased in subordinate male hamsters compared with the nonstressed controls (P < 0.05 for each; Fig. 4). WAT masses did not differ between nonstressed control and dominant male hamsters. Finally, there was no effect on testes mass among the groups (Table 1).


Figure 4
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  		Fig. 4. Mesenteric (MWAT), inguinal (IWAT), retroperitoneal (RWAT), and epididymal (EWAT) white adipose tissue (WAT) masses of control (n = 9), subordinate (n = 8), and dominant (n = 9) hamsters in experiment 1. Values are means ± SE. Nonshared letters (a, b) indicate statistically significant differences (P < 0.05).

 

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  		Table 1. Serum hormone concentration and paired testes mass: experiment 1

 
Serum T and leptin concentrations. Serum T concentrations did not differ among the groups (Table 1). Serum leptin concentrations were significantly greater in subordinate than in nonstressed control and dominant hamsters (P < 0.05 for each; Table 1).

Carcass composition. There was no significant difference among any of the groups in absolute carcass FFDM or water content (Fig. 5A); however, absolute carcass lipid content was significantly greater in subordinate than in nonstressed control and dominant male hamsters (P < 0.05 for each; Fig. 5A). Dominant hamsters had a greater percent carcass water content and a lower percentage of carcass lipid content than nonstressed control and subordinate male hamsters (P < 0.05 for each; Fig. 5B). There was no difference in percentage of carcass FFDM among any of the groups.


Figure 5
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  		Fig. 5. A: absolute carcass components of control (n = 9), subordinate (n = 8), and dominant (n = 9) hamsters in experiment 1. FFDM, fat-free dry mass. B: relative percent carcass component of control (n = 9), subordinate (n = 8), and dominant (n = 9) hamsters in experiment 1. Values are means ± SE. Nonshared letters (a, b) indicate statistically significant differences (P < 0.05).

 
Experiment 2: Does Footshock Stress Increase Food Intake, Body Mass, and Adiposity in Male Syrian Hamsters?

Body mass, food intake, and feed efficiency. One animal from the control group was eliminated from statistical analyses because of an unexplainable loss (i.e., >10 g) of body mass. From day 15 until the end of the study, footshock stress induced a significant increase in body mass compared with nonstressed controls (P < 0.05 for each; Fig. 6A), whereas social defeat did not until day 19. The cumulative body mass was significantly greater in subordinate and footshock groups than in the nonstressed controls (P < 0.05 for each; Fig. 6B). Despite the increase in body mass in the footshock and subordinate groups, there was no significant difference in food intake among any of the groups (data not shown). Accordingly, feed efficiency was significantly higher in the footshock and subordinate groups than in the nonstressed controls (P < 0.05 each; Fig. 7).


Figure 6
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  		Fig. 6. A: absolute body mass of control (n = 5), subordinate (n = 7), and footshocked (n = 7) hamsters in experiment 2. Arrows, days of introduction of stress for subordinate and footshock groups only (i.e., days 7, 8, 9, and 10). B: cumulative body mass increase relative to baseline of control (n = 5), subordinate (n = 7), and footshocked (n = 7) hamsters in experiment 2. Values are means ± SE. *P < 0.05, subordinate vs. footshock vs. control. #P < 0.05, footshock vs. control. Nonshared letters (a, b) indicate statistically shared significant differences (P < 0.05).

 

Figure 7
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  		Fig. 7. Feed efficiency of control (n = 5), subordinate (n = 7), and footshocked (n = 6) male hamsters. Values are means ± SE. Nonshared letters (a, b) indicate statistically significant differences (P < 0.05).

 
Fat pad and testes masses. MWAT mass was significantly increased in footshock and subordinate groups compared with nonstressed controls (P < 0.05; Fig. 8). In addition, EWAT mass was significantly increased in subordinate hamsters compared with nonstressed controls (P < 0.05; Fig. 8). There was no difference in IWAT and EWAT mass among any of the groups (Fig. 8). As in experiment 1, testes mass was not different among the groups (Table 2).


Figure 8
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  		Fig. 8. MWAT, IWAT, RWAT, and EWAT masses of control (n = 5), subordinate (n = 7), and footshocked (n = 7) hamsters in experiment 2. Values are means ± SE. Nonshared letters (a, b) indicate statistically significant differences (P < 0.05).

 

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  		Table 2. Serum hormone concentration and testes mass: experiment 2

 
Serum leptin and insulin concentrations. Serum leptin concentration was significantly greater in subordinate than in footshock and nonstressed control animals (P < 0.05 for each; Table 2); moreover, serum leptin concentration was significantly greater in the footshock than in the nonstressed control animals (P < 0.05; Table 2). Serum insulin concentration was also significantly greater in subordinate than in nonstressed control animals (P < 0.05). There was no significant difference in serum insulin levels between footshock and nonstressed control animals (Table 2).

Carcass composition. There were no significant differences in absolute carcass water or FFDM mass among any of the groups (Fig. 9A). However, carcass lipid content was significantly increased in subordinate hamsters compared with nonstressed controls (P < 0.05; Fig. 9A). There was no difference in carcass lipid between footshock and nonstressed control animals nor was there an affect of any experimental treatment on relative carcass composition for any component (data not shown).


Figure 9
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  		Fig. 9. Absolute carcass composition of control (n = 5), subordinate (n = 7), and footshocked (n = 7) hamsters in experiment 2. Values are means ± SE. Nonshared letters (a, b) indicate statistically significant differences (P < 0.05).

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
The present experiments support and extend our previous finding (17) that subordinate Syrian hamsters exhibit increases in food intake and body mass, as well as increases in several fat pad masses, compared with nonstressed controls. The results of the present study show persistently increased body mass and WAT pad masses, increased total carcass lipid, and increased serum leptin concentrations in Syrian hamsters exposed to social defeat or footshock compared with nonstressed controls. Subordinate animals also ate more and had greater feed efficiencies, suggesting decreased energy expenditure, than the dominant or nonstressed control hamsters. Although feed efficiencies were higher and increases in body mass gain were greater in the dominant than in the control animals, the dominant hamsters did not have significantly larger WAT pad masses, increased total carcass lipid, or larger increases in carcass lipid than the controls. Thus we have demonstrated, for the first time, social stress-induced increases in WAT pad masses as well as carcass lipid specifically in subordinate hamsters, and not in dominant hamsters, after agonistic encounters. Moreover, we have demonstrated that a nonsocial stressor, footshock, similarly increased body mass, feed efficiency, and some WAT pad (i.e., MWAT) masses but not total carcass lipid. By contrast, with footshock stress, it seems that social defeat produces a more marked increase in adiposity, with increases in RWAT and EWAT, as well as overall body fat, as reflected in the significantly increased carcass lipid compared with nonstressed controls.

Animals exposed to defeat or footshock stress exhibited a significant increase in body mass. This increased body mass was largely reflected as increased fat pad mass growth; however, the stress-induced increases in fat pad mass growth were not specific or consistent in all instances. For example, in experiment 1, animals exposed to social defeat exhibited significantly increased RWAT and EWAT fat pad masses relative to nonstressed controls; in experiment 2, however, defeat triggered increases in MWAT and EWAT fat pad mass growth. On the other hand, only MWAT was significantly increased in animals exposed to footshock compared with nonstressed controls. The variation in defeat- and footshock-induced fat pad increases may be due to subtle differences in the intensity of the stressful encounters between experiments. In addition, although the increase in body mass in the subordinate animals relative to the nonstressed controls was more consistently due to increased carcass lipid, footshock stress did not induce a similar increase. This finding suggests that the stress-induced changes in adiposity depend on the nature of the stressor. Nonetheless, the defeat-induced increases in body mass and adiposity in the present study are consistent with our previous findings of increases in body and fat pad mass and overall adiposity in Syrian hamsters with acute exposure (7 min over 4 days) to social stress (17).

Perhaps an even more notable finding of this study is the marked difference in distribution of adiposity depending on social status. For instance, although the dominant and subordinate animals did not differ in their absolute body mass, there were significant differences in fat pad mass growth and carcass composition between the two groups. More specifically, defeat triggered increases in all fat pad (i.e., MWAT, IWAT, RWAT, and EWAT) masses in subordinate hamsters compared with their dominant counterparts. Thus, although thoroughly involved in the agonistic encounter, the dominant hamsters had body fat distributions (i.e., fat pad masses) that were most similar to those of nonstressed controls. In addition, although dominant and subordinate hamsters had agonistic encounter-related increases in body mass, dominant hamsters appeared to achieve this increase by a redistribution of their carcass composition, significantly decreasing carcass lipid while increasing their percentage of carcass water, whereas subordinates increased carcass lipid only, although this could be definitively known only if the initial carcass composition had been assessed. One possible explanation for these differences in distribution of carcass composition might be increased activity levels of dominant hamsters compared with subordinate hamsters. Consistent with this notion, dominant mice have increased physical activity within an open field arena (5) and during an agonistic encounter (4). In the present study, although activity levels were not directly measured during the agonistic encounter, we did not observe any differences in activity during the agonistic encounter; however, activity might have been increased after the encounter. The underlying mechanism for this differential effect on carcass composition depending on territorial status is unknown.

Although subordinate animals in experiment 1 significantly increased their food intake compared with nonstressed controls, this stress-induced increase in food intake was not consistent across experiments. For example, in experiment 2, although animals exposed to footshock or defeat had a significant increase in body mass relative to nonstressed controls, the increase in food intake was not significant. This finding suggests that increased food intake is not necessary to achieve the stress-induced increases in body mass. Although we did not directly measure energy expenditure, feed efficiency reflects the relation between energy intake and energy stored and, therefore, can reflect changes in energy expenditure. The significantly higher feed efficiencies in animals exposed to social defeat or footshock stress suggest a decrease in energy expenditure, especially given the increases in lipid deposition, the energy cost of which is twice that of similar increases in lean mass, in this group. Thus the increased body and lipid masses observed in animals that were exposed to social defeat or footshock might be due to a decrease in energy expenditure, although the mechanism for this apparent stress-induced decrease in metabolic activity is unknown.

The relation between serum T concentrations and aggression is varied in the literature. For example, many studies report a positive correlation between T concentrations and aggression in a number of species (15, 19, 35). The data from the present study, along with others (13, 27, 39), do not support this association. The conflicting findings on whether aggression is dependent on increased circulating T concentrations might be due to species differences as well as the duration, intensity, and type of the agonistic encounters.

Leptin is primarily synthesized by WAT approximately in proportion to the amount of body fat (for review see Ref. 32), although there are increasing numbers of exceptions (41). Consistent with the notion that leptin serves as an adiposity signal, in both experiments, circulating serum leptin concentrations were significantly elevated in subordinate hamsters, in which total carcass lipid was significantly greater and mass of several WAT pads was increased compared with nonstressed control or dominant hamsters. In experiment 2, insulin [which is also hypothesized to be an adiposity signal (for review see Ref. 32)] was significantly increased only in the subordinate hamsters, a finding that is consistent with their greater adiposity. That is, total carcass lipid only was significantly increased in subordinates compared with nonstressed controls and was reflected as significantly increased MWAT and EWAT. On the other hand, the total carcass lipid of the shocked hamsters was not significantly different from that of the nonstressed controls, and only MWAT mass was increased. It may be that less adiposity of the shocked than the subordinate hamsters did not result in as robust a synthesis/secretion of insulin relative to their body fat.

In the present study, we did not measure glucocorticoids (i.e., cortisol or corticosterone), because the terminal measures were collected ~10 days after the cessation of the final stressor; thus differences in circulating concentrations of glucocorticoids between the stressed and nonstressed groups would not be expected at this time. Other studies from our laboratory have shown that exposure to defeat and footshock results in marked, transitory elevations in circulating glucocorticoid concentrations in Syrian hamsters (25). Our recent study examining the effects of social defeat on body mass and adiposity (17) did not reveal a significant difference in cortisol concentrations between animals that were exposed to social defeat and their nonstressed controls. Again, this is probably attributable to the time lag between collection of the terminal measures and cessation of the stressor. It is entirely possible that transitory increases in circulating glucocorticoids do contribute to the increase in visceral adiposity in stressed hamsters, and future studies could examine this hypothesis.

Collectively, the present data demonstrate that social stress in Syrian hamsters promotes adiposity in the subordinate, but not the dominant, hamster. Moreover, we found for the first time that promotion of adiposity and related responses by a nonsocial stressor, footshock, was somewhat similar to that by the social stressor. It is noteworthy that of the WAT pads examined, both types of stressors significantly stimulated the growth of MWAT, a visceral WAT pad, and this was the only fat pad that significantly increased in size with footshock. Part of the underlying mechanism for the differential stimulation of MWAT vs. other WAT pads may be a greater density of glucocorticoid receptors (16), which, when stimulated by the stress-induced release of glucocorticoids, facilitates lipid accumulation. The defeat-induced stimulation of MWAT replicates our finding from a previous study using this stressor (17). Because chronic stress has been associated with an accumulation of excess body fat, particularly in the abdominal region in humans (49), and because excess abdominal tissue is highly correlated with the deleterious comorbidities associated with obesity (34), the use of these stressors with Syrian hamsters may be a useful model for the human condition that is not offered by other rodent models.


   GRANTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
This research was supported, in part, by National Institutes of Health Grants R01 DK-35254 (to T. J. Bartness) and R01 MH-62044 (to K. L. Huhman) and National Science Foundation Science and Technology Centers Program Agreement IBN-9876754.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Ryan Early for statistical assistance, Susan Lackey (Endocrine Core at Emory University, Atlanta, GA) for performing the testosterone, leptin, and insulin assays, and Dr. Ruth Harris for helpful discussions.


   FOOTNOTES
 

Address for reprint requests and other correspondence: K. L. Huhman, Center for Behavioral Neuroscience, Georgia State Univ., PO Box 3966, Atlanta, GA 30302-3966 (e-mail: khuhman{at}gsu.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
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